{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T02:56:33Z","timestamp":1787021793526,"version":"build-2736575974"},"reference-count":34,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2024,9,12]],"date-time":"2024-09-12T00:00:00Z","timestamp":1726099200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["Grant Nos. 32330011 and 32270507"],"award-info":[{"award-number":["Grant Nos. 32330011 and 32270507"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>\n                    Holometabolous insects undergo morphological remodeling from larvae to pupae and to adults with typical changes in the cuticle; however, the mechanism is unclear. Using the lepidopteran agricultural insect\n                    <jats:italic>Helicoverpa armigera<\/jats:italic>\n                    , cotton bollworm, as a model, we revealed that the transcription factor RUNT-like (encoded by\n                    <jats:italic>Runt-like<\/jats:italic>\n                    ) regulates the development of the pupal cuticle via promoting a pupal cuticle protein gene (\n                    <jats:italic>HaPcp<\/jats:italic>\n                    ) expression. The\n                    <jats:italic>HaPcp<\/jats:italic>\n                    was highly expressed in the epidermis and wing during metamorphosis and was found being involved in pupal cuticle development by RNA interference (RNAi) analysis in larvae.\n                    <jats:italic>Runt-like<\/jats:italic>\n                    was also strongly upregulated in the epidermis and wing during metamorphosis. Knockdown of\n                    <jats:italic>Runt-like<\/jats:italic>\n                    produced similar phenomena, a failure of abdomen yellow envelope and wing formation, to those following\n                    <jats:italic>HaPcp<\/jats:italic>\n                    knockdown. The insect molting hormone 20-hydroxyecdysonen (20E) upregulated\n                    <jats:italic>HaPcp<\/jats:italic>\n                    transcription via RUNT-like. 20E upregulated\n                    <jats:italic>Runt-like<\/jats:italic>\n                    transcription via nuclear receptor EcR and the transcription factor FOXO. Together, RUNT-like and HaPCP are involved in pupal cuticle development during metamorphosis under 20E regulation.\n                  <\/jats:p>","DOI":"10.1371\/journal.pgen.1011393","type":"journal-article","created":{"date-parts":[[2024,9,12]],"date-time":"2024-09-12T13:39:57Z","timestamp":1726148397000},"page":"e1011393","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["The transcription factor RUNT-like regulates pupal cuticle development via promoting a pupal cuticle protein transcription"],"prefix":"10.1371","volume":"20","author":[{"given":"Ke-Yan","family":"Jin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao-Pei","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Qin","family":"Di","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Meng","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin-Xing","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1809-4730","authenticated-orcid":true,"given":"Xiao-Fan","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,9,12]]},"reference":[{"issue":"6","key":"pgen.1011393.ref001","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1016\/S2095-3119(19)62860-1","article-title":"Progress in understanding hormonal regulation during the postembryonic development of Helicoverpa armigera","volume":"19","author":"XF Zhao","year":"2020","journal-title":"J Integr Agr"},{"issue":"4\u20135","key":"pgen.1011393.ref002","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1016\/S0022-1910(00)00123-2","article-title":"The Wigglesworth Lecture: Insects for studying fundamental problems in biology","volume":"47","author":"M. Locke","year":"2001","journal-title":"J Insect Physiol"},{"issue":"5","key":"pgen.1011393.ref003","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1016\/j.ibmb.2010.03.003","article-title":"Recent advances in understanding mechanisms of insect cuticle differentiation","volume":"40","author":"B. Moussian","year":"2010","journal-title":"Insect Biochem Mol Biol"},{"key":"pgen.1011393.ref004","doi-asserted-by":"crossref","first-page":"103206","DOI":"10.1016\/j.ibmb.2019.103206","article-title":"The wing-specific cuticular protein LmACP7 is essential for normal wing morphogenesis in the migratory locust","volume":"112","author":"X Zhao","year":"2019","journal-title":"Insect Biochem Mol Biol"},{"issue":"6","key":"pgen.1011393.ref005","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1111\/1744-7917.12231","article-title":"Analysis of expression and chitin-binding activity of the wing disc cuticle protein BmWCP4 in the silkworm, Bombyx mori","volume":"23","author":"HM Deng","year":"2016","journal-title":"Insect science"},{"issue":"9","key":"pgen.1011393.ref006","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1016\/j.ibmb.2009.06.007","article-title":"betaFTZ-F1 and Broad-Complex positively regulate the transcription of the wing cuticle protein gene, BMWCP5, in wing discs of Bombyx mori","volume":"39","author":"HB Wang","year":"2009","journal-title":"Insect Biochem Mol Biol"},{"issue":"10","key":"pgen.1011393.ref007","doi-asserted-by":"crossref","first-page":"3087","DOI":"10.1534\/g3.119.400581","article-title":"An RNAi screen for genes required for growth of Drosophila wing tissue","volume":"9","author":"MD Rotelli","year":"2019","journal-title":"G3 (Bethesda, Md)"},{"issue":"Pt A","key":"pgen.1011393.ref008","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.mod.2016.10.003","article-title":"Forces shaping the Drosophila wing","volume":"144","author":"MC Diaz de la Loza","year":"2017","journal-title":"Mech Develop"},{"issue":"23","key":"pgen.1011393.ref009","doi-asserted-by":"crossref","first-page":"R1252","DOI":"10.1016\/j.cub.2019.10.009","article-title":"The evolution of insect metamorphosis","volume":"29","author":"JW Truman","year":"2019","journal-title":"Curr Biol"},{"issue":"5","key":"pgen.1011393.ref010","doi-asserted-by":"crossref","first-page":"1170","DOI":"10.1080\/15548627.2020.1752497","article-title":"Autophagy triggers CTSD (cathepsin D) maturation and localization inside cells to promote apoptosis","volume":"17","author":"YQ Di","year":"2021","journal-title":"Autophagy"},{"key":"pgen.1011393.ref011","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2121-11-1","article-title":"Function of nuclear transport factor 2 and Ran in the 20E signal transduction pathway in the cotton bollworm, Helicoverpa armigera","volume":"11","author":"HJ He","year":"2010","journal-title":"BMC cell biology"},{"issue":"6","key":"pgen.1011393.ref012","first-page":"1005","article-title":"20-hydroxyecdysone activates Forkhead box O to promote proteolysis during molting","volume":"143","author":"MJ Cai","year":"2016","journal-title":"Development"},{"issue":"3","key":"pgen.1011393.ref013","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.ibmb.2009.12.005","article-title":"The regulation of expression of insect cuticle protein genes","volume":"40","author":"JP Charles","year":"2010","journal-title":"Insect Biochem Mol Biol"},{"issue":"1","key":"pgen.1011393.ref014","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.jmb.2012.10.020","article-title":"The binding of multiple nuclear receptors to a single regulatory region is important for the proper expression of EDG84A in Drosophila melanogaster","volume":"425","author":"K Akagi","year":"2013","journal-title":"J Mol Biol"},{"key":"pgen.1011393.ref015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ibmb.2015.11.008","article-title":"Ecdysteroid promotes cell cycle progression in the Bombyx wing disc through activation of c-Myc","volume":"70","author":"M Moriyama","year":"2016","journal-title":"Insect Biochem Mol Biol"},{"issue":"1","key":"pgen.1011393.ref016","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.bcmd.2009.05.001","article-title":"RUNX factors in development: lessons from invertebrate model systems","volume":"43","author":"T Braun","year":"2009","journal-title":"Blood cells, molecules & diseases"},{"issue":"10","key":"pgen.1011393.ref017","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1007\/s00427-008-0244-x","article-title":"Conserved cluster organization of insect Runx genes","volume":"218","author":"R Bao","year":"2008","journal-title":"Dev Genes Evol"},{"key":"pgen.1011393.ref018","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-981-10-3233-2_1","article-title":"RUNX in Invertebrates","volume":"962","author":"S Hughes","year":"2017","journal-title":"Advances in experimental medicine and biology"},{"issue":"6","key":"pgen.1011393.ref019","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1002\/ijc.27964","article-title":"RUNX family: Regulation and diversification of roles through interacting proteins","volume":"132","author":"LS Chuang","year":"2013","journal-title":"Int J Cancer"},{"issue":"10","key":"pgen.1011393.ref020","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1016\/S0969-2126(00)80058-1","article-title":"The Ig fold of the core binding factor alpha Runt domain is a member of a family of structurally and functionally related Ig-fold DNA-binding domains","volume":"7","author":"MJ Berardi","year":"1999","journal-title":"Structure (London, England: 1993)"},{"issue":"4","key":"pgen.1011393.ref021","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/S1065-6995(03)00018-0","article-title":"Runx transcription factors and the developmental balance between cell proliferation and differentiation","volume":"27","author":"JA Coffman","year":"2003","journal-title":"Cell Biol Int"},{"issue":"2","key":"pgen.1011393.ref022","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1002\/arch.20261","article-title":"Cloning and characterization of Bmrunt from the silkworm Bombyx mori during embryonic development","volume":"69","author":"W Liu","year":"2008","journal-title":"Archives of insect biochemistry and physiology"},{"issue":"5","key":"pgen.1011393.ref023","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1006\/scdb.2000.0185","article-title":"Runt and Lozenge function in Drosophila development","volume":"11","author":"J Canon","year":"2000","journal-title":"Seminars in cell & developmental biology"},{"issue":"2","key":"pgen.1011393.ref024","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/nrm3507","article-title":"FOXOs: signalling integrators for homeostasis maintenance","volume":"14","author":"A Eijkelenboom","year":"2013","journal-title":"Nat Rev Mol Cell Bio"},{"issue":"19","key":"pgen.1011393.ref025","doi-asserted-by":"crossref","first-page":"13026","DOI":"10.1074\/jbc.M113.547018","article-title":"Phospholipase C\u03b31 connects the cell membrane pathway to the nuclear receptor pathway in insect steroid hormone signaling","volume":"289","author":"W Liu","year":"2014","journal-title":"J of Biol Chem"},{"issue":"11","key":"pgen.1011393.ref026","first-page":"1083","article-title":"A conserved domain in arthropod cuticular proteins binds chitin","volume":"31","author":"JE Rebers","year":"2001","journal-title":"Insect Biochem Molec"},{"issue":"7","key":"pgen.1011393.ref027","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1016\/S0965-1748(00)00029-1","article-title":"Studies on proteins in post-ecdysial nymphal cuticle of locust, and cockroach","volume":"30","author":"SO Andersen","year":"2000","journal-title":"Insect Biochem Molec"},{"issue":"2","key":"pgen.1011393.ref028","doi-asserted-by":"crossref","first-page":"e1004963","DOI":"10.1371\/journal.pgen.1004963","article-title":"RR-1 cuticular protein TcCPR4 is required for formation of pore canals in rigid cuticle","volume":"11","author":"MY Noh","year":"2015","journal-title":"Plos Genet"},{"issue":"6","key":"pgen.1011393.ref029","doi-asserted-by":"crossref","first-page":"583","DOI":"10.2108\/zs160105","article-title":"An RNAi screen for genes involved in nanoscale protrusion formation on corneal lens in","volume":"33","author":"R Minami","year":"2016","journal-title":"Zool Sci"},{"key":"pgen.1011393.ref030","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1186\/1471-2164-9-396","article-title":"Catalogue of epidermal genes: genes expressed in the epidermis during larval molt of the silkworm Bombyx mori","volume":"9","author":"S Okamoto","year":"2008","journal-title":"BMC genomics"},{"issue":"2","key":"pgen.1011393.ref031","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1093\/genetics\/120.2.465","article-title":"Prepupal differentiation of Drosophila imaginal discs: identification of four genes whose transcripts accumulate in response to a pulse of 20-hydroxyecdysone","volume":"120","author":"K Fechtel","year":"1988","journal-title":"Genetics"},{"issue":"9","key":"pgen.1011393.ref032","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/j.ibmb.2009.06.008","article-title":"Activation of BMWCP10 promoter and regulation by BR-C Z2 in wing disc of Bombyx mori","volume":"39","author":"HB Wang","year":"2009","journal-title":"Insect Biochem Mol Biol"},{"issue":"2","key":"pgen.1011393.ref033","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/s00427-012-0392-x","article-title":"Ecdysone-responsive transcription factors determine the expression region of target cuticular protein genes in the epidermis of Bombyx mori","volume":"222","author":"MS Ali","year":"2012","journal-title":"Dev Genes Evol"},{"issue":"34","key":"pgen.1011393.ref034","first-page":"E7121","article-title":"Protein kinase C delta phosphorylates ecdysone receptor B1 to promote gene expression and apoptosis under 20-hydroxyecdysone regulation","volume":"114","author":"CH Chen","year":"2017","journal-title":"P Natl Acad Sci USA"}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011393","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,12]],"date-time":"2024-09-12T13:40:25Z","timestamp":1726148425000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011393"}},"subtitle":[],"editor":[{"given":"Subba Reddy","family":"Palli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,9,12]]},"references-count":34,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,9,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1011393","relation":{},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,12]]}}}