{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,9]],"date-time":"2026-05-09T11:19:09Z","timestamp":1778325549319,"version":"3.51.4"},"reference-count":33,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2022,9,1]],"date-time":"2022-09-01T00:00:00Z","timestamp":1661990400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2022,9,1]],"date-time":"2022-09-01T00:00:00Z","timestamp":1661990400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/501100004085","name":"Ministry of Education, Science and Technology","doi-asserted-by":"publisher","award":["NRF-2015R1A5A1009024"],"award-info":[{"award-number":["NRF-2015R1A5A1009024"]}],"id":[{"id":"10.13039\/501100004085","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002701","name":"Ministry of Education","doi-asserted-by":"publisher","award":["NRF-2021R1A6A1A10045235"],"award-info":[{"award-number":["NRF-2021R1A6A1A10045235"]}],"id":[{"id":"10.13039\/501100002701","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell. Mol. Life Sci."],"published-print":{"date-parts":[[2022,9]]},"DOI":"10.1007\/s00018-022-04535-4","type":"journal-article","created":{"date-parts":[[2022,9,4]],"date-time":"2022-09-04T09:02:41Z","timestamp":1662282161000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Small leucine zipper protein functions as a modulator for metabolic reprogramming of colorectal cancer cells by inducing nutrient stress-mediated autophagy"],"prefix":"10.1007","volume":"79","author":[{"given":"Suhyun","family":"Kim","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Minseok","family":"Oh","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Minsoo","family":"Kang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7609-9719","authenticated-orcid":false,"given":"Jesang","family":"Ko","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,9,4]]},"reference":[{"key":"4535_CR1","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1186\/1476-4598-7-72","volume":"7","author":"C Denkert","year":"2008","unstructured":"Denkert C, Budczies J, Weichert W, Wohlgemuth G, Scholz M et al (2008) Metabolite profiling of human colon carcinoma\u2013deregulation of TCA cycle and amino acid turnover. Mol Cancer 7:72. https:\/\/doi.org\/10.1186\/1476-4598-7-72","journal-title":"Mol Cancer"},{"key":"4535_CR2","doi-asserted-by":"publisher","DOI":"10.1074\/mcp.M900551-MCP200","author":"ES Ong","year":"2010","unstructured":"Ong ES, Zou L, Li S, Cheah PY, Eu KW et al (2010) Metabolic profiling in colorectal cancer reveals signature metabolic shifts during tumorigenesis. Mol Cell Proteom. https:\/\/doi.org\/10.1074\/mcp.M900551-MCP200","journal-title":"Mol Cell Proteom"},{"issue":"1","key":"4535_CR3","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.cmet.2015.12.006","volume":"23","author":"NN Pavlova","year":"2016","unstructured":"Pavlova NN, Thompson CB (2016) The emerging hallmarks of cancer metabolism. Cell Metab 23(1):27\u201347. https:\/\/doi.org\/10.1016\/j.cmet.2015.12.006","journal-title":"Cell Metab"},{"key":"4535_CR4","doi-asserted-by":"publisher","DOI":"10.3390\/ijms22126262","author":"M Nenkov","year":"2021","unstructured":"Nenkov M, Ma Y, Gassler N, Chen Y (2021) Metabolic reprogramming of colorectal cancer cells and the microenvironment: implication for therapy. Int J Mol Sci. https:\/\/doi.org\/10.3390\/ijms22126262","journal-title":"Int J Mol Sci"},{"issue":"1","key":"4535_CR5","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1038\/s41416-019-0477-7","volume":"121","author":"T Charitou","year":"2019","unstructured":"Charitou T, Srihari S, Lynn MA, Jarboui MA, Fasterius E et al (2019) Transcriptional and metabolic rewiring of colorectal cancer cells expressing the oncogenic KRAS(G13D) mutation. Br J Cancer 121(1):37\u201350. https:\/\/doi.org\/10.1038\/s41416-019-0477-7","journal-title":"Br J Cancer"},{"issue":"3","key":"4535_CR6","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/j.ccr.2010.08.009","volume":"18","author":"JB Wang","year":"2010","unstructured":"Wang JB, Erickson JW, Fuji R, Ramachandran S, Gao P et al (2010) Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell 18(3):207\u2013219. https:\/\/doi.org\/10.1016\/j.ccr.2010.08.009","journal-title":"Cancer Cell"},{"issue":"2","key":"4535_CR7","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1016\/j.cell.2013.09.025","volume":"155","author":"WJ Israelsen","year":"2013","unstructured":"Israelsen WJ, Dayton TL, Davidson SM, Fiske BP, Hosios AM et al (2013) PKM2 isoform-specific deletion reveals a differential requirement for pyruvate kinase in tumor cells. Cell 155(2):397\u2013409. https:\/\/doi.org\/10.1016\/j.cell.2013.09.025","journal-title":"Cell"},{"issue":"37","key":"4535_CR8","doi-asserted-by":"publisher","first-page":"E7697","DOI":"10.1073\/pnas.1710366114","volume":"114","author":"K Satoh","year":"2017","unstructured":"Satoh K, Yachida S, Sugimoto M, Oshima M, Nakagawa T et al (2017) Global metabolic reprogramming of colorectal cancer occurs at adenoma stage and is induced by MYC. Proc Natl Acad Sci U S A 114(37):E7697\u2013E7706. https:\/\/doi.org\/10.1073\/pnas.1710366114","journal-title":"Proc Natl Acad Sci U S A"},{"key":"4535_CR9","doi-asserted-by":"publisher","DOI":"10.3390\/cells8111349","author":"SN Devenport","year":"2019","unstructured":"Devenport SN, Shah YM (2019) Functions and implications of autophagy in colon cancer. Cells. https:\/\/doi.org\/10.3390\/cells8111349","journal-title":"Cells"},{"issue":"8","key":"4535_CR10","doi-asserted-by":"publisher","first-page":"1062","DOI":"10.1038\/ncb3206","volume":"17","author":"J Levy","year":"2015","unstructured":"Levy J, Cacheux W, Bara MA, L\u2019Hermitte A, Lepage P et al (2015) Intestinal inhibition of Atg7 prevents tumour initiation through a microbiome-influenced immune response and suppresses tumour growth. Nat Cell Biol 17(8):1062\u20131073. https:\/\/doi.org\/10.1038\/ncb3206","journal-title":"Nat Cell Biol"},{"issue":"12","key":"4535_CR11","doi-asserted-by":"publisher","first-page":"1148","DOI":"10.1038\/s41419-018-1113-9","volume":"9","author":"T Xiao","year":"2018","unstructured":"Xiao T, Zhu W, Huang W, Lu SS, Li XH et al (2018) RACK1 promotes tumorigenicity of colon cancer by inducing cell autophagy. Cell Death Dis 9(12):1148. https:\/\/doi.org\/10.1038\/s41419-018-1113-9","journal-title":"Cell Death Dis"},{"issue":"1","key":"4535_CR12","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/j.bbrc.2018.01.017","volume":"496","author":"J Kim","year":"2018","unstructured":"Kim J, Choi S, Kim JO, Kim KK (2018) Autophagy-mediated upregulation of cytoplasmic claudin 1 stimulates the degradation of SQSTM1\/p62 under starvation. Biochem Biophys Res Commun 496(1):159\u2013166. https:\/\/doi.org\/10.1016\/j.bbrc.2018.01.017","journal-title":"Biochem Biophys Res Commun"},{"issue":"11","key":"4535_CR13","doi-asserted-by":"publisher","first-page":"1272","DOI":"10.1158\/2159-8290.CD-13-0397","volume":"3","author":"AM Strohecker","year":"2013","unstructured":"Strohecker AM, Guo JY, Karsli-Uzunbas G, Price SM, Chen GJ et al (2013) Autophagy sustains mitochondrial glutamine metabolism and growth of BrafV600E-driven lung tumors. Cancer Discov 3(11):1272\u20131285. https:\/\/doi.org\/10.1158\/2159-8290.CD-13-0397","journal-title":"Cancer Discov"},{"issue":"7","key":"4535_CR14","doi-asserted-by":"publisher","first-page":"1179","DOI":"10.4161\/auto.28679","volume":"10","author":"MF Wei","year":"2014","unstructured":"Wei MF, Chen MW, Chen KC, Lou PJ, Lin SY et al (2014) Autophagy promotes resistance to photodynamic therapy-induced apoptosis selectively in colorectal cancer stem-like cells. Autophagy 10(7):1179\u20131192. https:\/\/doi.org\/10.4161\/auto.28679","journal-title":"Autophagy"},{"issue":"34","key":"4535_CR15","doi-asserted-by":"publisher","first-page":"13561","DOI":"10.1073\/pnas.1121572109","volume":"109","author":"K Taguchi","year":"2012","unstructured":"Taguchi K, Fujikawa N, Komatsu M, Ishii T, Unno M et al (2012) Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc Natl Acad Sci U S A 109(34):13561\u201313566. https:\/\/doi.org\/10.1073\/pnas.1121572109","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"11","key":"4535_CR16","doi-asserted-by":"publisher","first-page":"1746","DOI":"10.1210\/me.2009-0009","volume":"23","author":"H Kang","year":"2009","unstructured":"Kang H, Kim YS, Ko J (2009) A novel isoform of human LZIP negatively regulates the transactivation of the glucocorticoid receptor. Mol Endocrinol 23(11):1746\u20131757. https:\/\/doi.org\/10.1210\/me.2009-0009","journal-title":"Mol Endocrinol"},{"issue":"2","key":"4535_CR17","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1038\/onc.2013.538","volume":"34","author":"Y Kim","year":"2015","unstructured":"Kim Y, Kim J, Jang SW, Ko J (2015) The role of sLZIP in cyclin D3-mediated negative regulation of androgen receptor transactivation and its involvement in prostate cancer. Oncogene 34(2):226\u2013236. https:\/\/doi.org\/10.1038\/onc.2013.538","journal-title":"Oncogene"},{"issue":"1","key":"4535_CR18","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1159\/000356658","volume":"33","author":"E Park","year":"2014","unstructured":"Park E, Kang H, Kim J, Ko J (2014) The role of sLZIP in transcriptional regulation of c-Jun and involvement in migration and invasion of cervical cancer cells. Cell Physiol Biochem 33(1):151\u2013164. https:\/\/doi.org\/10.1159\/000356658","journal-title":"Cell Physiol Biochem"},{"key":"4535_CR19","doi-asserted-by":"publisher","DOI":"10.1093\/jmcb\/mjaa069","author":"M Kang","year":"2020","unstructured":"Kang M, Han SK, Kim S, Park S, Jo Y et al (2020) Role of small leucine zipper protein in hepatic gluconeogenesis and metabolic disorder. J Mol Cell Biol. https:\/\/doi.org\/10.1093\/jmcb\/mjaa069","journal-title":"J Mol Cell Biol"},{"issue":"15","key":"4535_CR20","doi-asserted-by":"publisher","first-page":"1704","DOI":"10.1101\/gad.283416.116","volume":"30","author":"JY Guo","year":"2016","unstructured":"Guo JY, Teng X, Laddha SV, Ma S, Van Nostrand SC et al (2016) Autophagy provides metabolic substrates to maintain energy charge and nucleotide pools in Ras-driven lung cancer cells. Genes Dev 30(15):1704\u20131717. https:\/\/doi.org\/10.1101\/gad.283416.116","journal-title":"Genes Dev"},{"issue":"3","key":"4535_CR21","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1038\/cdd.2014.150","volume":"22","author":"G Filomeni","year":"2015","unstructured":"Filomeni G, De Zio D, Cecconi F (2015) Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ 22(3):377\u2013388. https:\/\/doi.org\/10.1038\/cdd.2014.150","journal-title":"Cell Death Differ"},{"issue":"8","key":"4535_CR22","doi-asserted-by":"publisher","first-page":"653","DOI":"10.1038\/gene.2011.43","volume":"12","author":"TH Agesen","year":"2011","unstructured":"Agesen TH, Berg M, Clancy T, Thiis-Evensen E, Cekaite L et al (2011) CLC and IFNAR1 are differentially expressed and a global immunity score is distinct between early- and late-onset colorectal cancer. Genes Immun 12(8):653\u2013662. https:\/\/doi.org\/10.1038\/gene.2011.43","journal-title":"Genes Immun"},{"issue":"2","key":"4535_CR23","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/j.ccr.2013.06.014","volume":"24","author":"KC Patra","year":"2013","unstructured":"Patra KC, Wang Q, Bhaskar PT, Miller L, Wang Z et al (2013) Hexokinase 2 is required for tumor initiation and maintenance and its systemic deletion is therapeutic in mouse models of cancer. Cancer Cell 24(2):213\u2013228. https:\/\/doi.org\/10.1016\/j.ccr.2013.06.014","journal-title":"Cancer Cell"},{"issue":"9","key":"4535_CR24","doi-asserted-by":"publisher","first-page":"3685","DOI":"10.1172\/JCI69741","volume":"123","author":"JR Doherty","year":"2013","unstructured":"Doherty JR, Cleveland JL (2013) Targeting lactate metabolism for cancer therapeutics. J Clin Invest 123(9):3685\u20133692. https:\/\/doi.org\/10.1172\/JCI69741","journal-title":"J Clin Invest"},{"issue":"4","key":"4535_CR25","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1007\/s10863-015-9612-1","volume":"47","author":"Y Sun","year":"2015","unstructured":"Sun Y, Liu Z, Zou X, Lan Y, Sun X et al (2015) Mechanisms underlying 3-bromopyruvate-induced cell death in colon cancer. J Bioenerg Biomembr 47(4):319\u2013329. https:\/\/doi.org\/10.1007\/s10863-015-9612-1","journal-title":"J Bioenerg Biomembr"},{"issue":"6009","key":"4535_CR26","doi-asserted-by":"publisher","first-page":"1344","DOI":"10.1126\/science.1193497","volume":"330","author":"JD Rabinowitz","year":"2010","unstructured":"Rabinowitz JD, White E (2010) Autophagy and metabolism. Science 330(6009):1344\u20131348. https:\/\/doi.org\/10.1126\/science.1193497","journal-title":"Science"},{"issue":"1","key":"4535_CR27","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1038\/s41392-020-0110-5","volume":"5","author":"L Yang","year":"2020","unstructured":"Yang L, Shi P, Zhao G, Xu J, Peng W et al (2020) Targeting cancer stem cell pathways for cancer therapy. Signal Transduct Target Ther 5(1):8. https:\/\/doi.org\/10.1038\/s41392-020-0110-5","journal-title":"Signal Transduct Target Ther"},{"key":"4535_CR28","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1186\/s12943-015-0449-3","volume":"14","author":"MC Yang","year":"2015","unstructured":"Yang MC, Wang HC, Hou YC, Tung HL, Chiu TJ et al (2015) Blockade of autophagy reduces pancreatic cancer stem cell activity and potentiates the tumoricidal effect of gemcitabine. Mol Cancer 14:179. https:\/\/doi.org\/10.1186\/s12943-015-0449-3","journal-title":"Mol Cancer"},{"key":"4535_CR29","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1016\/j.redox.2018.04.015","volume":"17","author":"IG Ryoo","year":"2018","unstructured":"Ryoo IG, Choi BH, Ku SK, Kwak MK (2018) High CD44 expression mediates p62-associated NFE2L2\/NRF2 activation in breast cancer stem cell-like cells: implications for cancer stem cell resistance. Redox Biol 17:246\u2013258. https:\/\/doi.org\/10.1016\/j.redox.2018.04.015","journal-title":"Redox Biol"},{"issue":"8","key":"4535_CR30","doi-asserted-by":"publisher","first-page":"1271","DOI":"10.1038\/cdd.2016.15","volume":"23","author":"JA Mason","year":"2016","unstructured":"Mason JA, Davison-Versagli CA, Leliaert AK, Pape DJ, McCallister C et al (2016) Oncogenic Ras differentially regulates metabolism and anoikis in extracellular matrix-detached cells. Cell Death Differ 23(8):1271\u20131282. https:\/\/doi.org\/10.1038\/cdd.2016.15","journal-title":"Cell Death Differ"},{"issue":"3","key":"4535_CR31","doi-asserted-by":"publisher","first-page":"797","DOI":"10.1091\/mbc.e07-10-1092","volume":"19","author":"C Fung","year":"2008","unstructured":"Fung C, Lock R, Gao S, Salas E, Debnath J (2008) Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 19(3):797\u2013806. https:\/\/doi.org\/10.1091\/mbc.e07-10-1092","journal-title":"Mol Biol Cell"},{"key":"4535_CR32","doi-asserted-by":"publisher","first-page":"13593","DOI":"10.1038\/ncomms13593","volume":"7","author":"ET Oh","year":"2016","unstructured":"Oh ET, Kim JW, Kim JM, Kim SJ, Lee JS et al (2016) NQO1 inhibits proteasome-mediated degradation of HIF-1alpha. Nat Commun 7:13593. https:\/\/doi.org\/10.1038\/ncomms13593","journal-title":"Nat Commun"},{"issue":"3","key":"4535_CR33","doi-asserted-by":"publisher","first-page":"1563","DOI":"10.21873\/anticanres.14916","volume":"41","author":"Y Hirose","year":"2021","unstructured":"Hirose Y, Sakata J, Kobayashi T, Miura K, Yuza K et al (2021) NQO1 as a marker of chemosensitivity and prognosis for colorectal liver metastasis. Anticancer Res 41(3):1563\u20131570. https:\/\/doi.org\/10.21873\/anticanres.14916","journal-title":"Anticancer Res"}],"container-title":["Cellular and Molecular Life Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00018-022-04535-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00018-022-04535-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00018-022-04535-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T12:44:31Z","timestamp":1663245871000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00018-022-04535-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9]]},"references-count":33,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2022,9]]}},"alternative-id":["4535"],"URL":"https:\/\/doi.org\/10.1007\/s00018-022-04535-4","relation":{},"ISSN":["1420-682X","1420-9071"],"issn-type":[{"value":"1420-682X","type":"print"},{"value":"1420-9071","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9]]},"assertion":[{"value":"14 June 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 August 2022","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 August 2022","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 September 2022","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"We declare that we have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}],"article-number":"505"}}