{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T04:14:33Z","timestamp":1781669673295,"version":"3.54.5"},"reference-count":52,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2023,1,31]],"date-time":"2023-01-31T00:00:00Z","timestamp":1675123200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institutes of Health, Eunice Kennedy Shriver National Institute of Child Health and Human Development","award":["R01HD109567"],"award-info":[{"award-number":["R01HD109567"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Adenomyosis is defined as the development of endometrial epithelial glands and stroma within the myometrial layer of the uterus. These \u201cectopic\u201d lesions share many cellular characteristics with endometriotic epithelial cells as well as endometrial adenocarcinoma cells, including enhanced proliferation, migration, invasion and progesterone resistance. We recently reported that the 60S acidic ribosomal protein P1, RPLP1, is up-regulated in endometriotic epithelial cells and lesion tissue where it plays a role in cell survival. To evaluate if a similar pattern of expression and function for RPLP1 exists in adenomyosis and endometrial cancer, we examined RPLP1 expression in adenomyosis and endometrial cancer tissue specimens and assessed its function in vitro using well-characterized cell lines. A total of 12 control endometrial biopsies and 20 eutopic endometrial and matched adenomyosis biopsies as well as 103 endometrial adenocarcinoma biopsies were evaluated for RPLP1 localization by immunohistochemistry. Endometrial adenocarcinoma cell lines, Ishikawa, HEC1A, HEC1B and AN3 were evaluated for RPLP1 protein and transcript expression, while in vitro function was evaluated by knocking down RPLP1 expression and assessing cell survival and migration. RPLP1 protein was up-regulated in eutopic epithelia as well as in adenomyosis lesions compared to eutopic endometria from control subjects. RPLP1 was also significantly up-regulated in endometrial adenocarcinoma tissue. Knockdown of RPLP1 in endometrial adenocarcinoma cell lines was associated with reduced cell survival and migration. RPLP1 expression is up-regulated in eutopic and ectopic adenomyotic epithelia as well as in the epithelia of endometrial cancer specimens. In vitro studies support an essential role for RPLP1 in mediating cell survival and migration, processes which are all involved in pathophysiology associated with both diseases.<\/jats:p>","DOI":"10.3390\/ijms24032690","type":"journal-article","created":{"date-parts":[[2023,2,1]],"date-time":"2023-02-01T02:29:03Z","timestamp":1675218543000},"page":"2690","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["RPLP1 Is Up-Regulated in Human Adenomyosis and Endometrial Adenocarcinoma Epithelial Cells and Is Essential for Cell Survival and Migration In Vitro"],"prefix":"10.3390","volume":"24","author":[{"given":"Riley","family":"Peterson","sequence":"first","affiliation":[{"name":"Department of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS 66160, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paige","family":"Minchella","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS 66160, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Cui","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, KS 66160, USA"},{"name":"Center for Reproductive Sciences, Institute for Reproductive and Developmental Sciences, University of Kansas Medical Center, Kansas City, KS 66160, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda","family":"Graham","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS 66160, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Warren B.","family":"Nothnick","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of Kansas Medical Center, Kansas City, KS 66160, USA"},{"name":"Center for Reproductive Sciences, Institute for Reproductive and Developmental Sciences, University of Kansas Medical Center, Kansas City, KS 66160, USA"},{"name":"Department of Obstetrics and Gynecology, University of Kansas Medical Center, Kansas City, KS 66160, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Kobayashi, H., Matsubara, S., and Imanaka, S. (2021). Clinicopathological features of different subtypes in adenomyosis: Focus on early lesions. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0254147"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"283","DOI":"10.12688\/f1000research.17242.1","article-title":"Recent advances in understanding and managing adenomyosis","volume":"8","author":"Vannuccini","year":"2019","journal-title":"F1000Research"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/j.fertnstert.2012.06.029","article-title":"Pathogenesis and pathophysiology of endometriosis","volume":"98","author":"Burney","year":"2012","journal-title":"Fertil. Steril."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1016\/S0140-6736(04)17403-5","article-title":"Endometriosis","volume":"364","author":"Giudice","year":"2004","journal-title":"Lancet"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1016\/j.tjog.2022.09.001","article-title":"Endometrial cancer: Part I. Basic concept","volume":"61","author":"Wang","year":"2022","journal-title":"Taiwan J. Obstet. Gynecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e8336","DOI":"10.1097\/MD.0000000000008336","article-title":"Malignant changes in adenomyosis in patients with endometrial adenocarcinoma: A case series","volume":"96","author":"Mao","year":"2017","journal-title":"Medicine"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"577","DOI":"10.3109\/09513590.2011.650761","article-title":"Molecular links between endometriosis and cancer","volume":"28","author":"Pollacco","year":"2012","journal-title":"Gynecol. Endocrinol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"807685","DOI":"10.3389\/fphys.2021.807685","article-title":"The potential relationship between environmental endocrine disruptor exposure and the development of endometriosis and adenomyosis","volume":"12","author":"Stephens","year":"2022","journal-title":"Front. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Hermens, M., van Altena, A.M., Velthuis, I., van de Laar, D.C.M., Bulten, J., van Vliet, H.A.A.M., Siebers, A.G., and Bekkers, R.L.M. (2021). Endometrial cancer incidence in endometriosis and adenomyosis. Cancers, 13.","DOI":"10.3390\/cancers13184592"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1093\/molehr\/gaz065","article-title":"60S acidic ribosomal protein P1 (RPLP1) is elevated in human endometriotic tissue and in a murine model of endometriosis and is essential for endometriotic epithelial cell survival in vitro","volume":"26","author":"Alali","year":"2020","journal-title":"Mol. Hum. Reprod."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/j.humpath.2010.04.020","article-title":"Expression of the ribosomal proteins Rplp0, Rplp1, and Rplp2 in gynecologic tumors","volume":"42","author":"Castellvi","year":"2011","journal-title":"Hum. Pathol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1046\/j.1432-1327.1999.00434.x","article-title":"Interaction of elongation factor eEF-2 with ribosomal P proteins","volume":"262","author":"Lavergne","year":"1999","journal-title":"Eur. J. Biochem."},{"key":"ref_13","first-page":"10184","article-title":"RPLP1 is highly expressed in hepatocellular carcinoma tissues and promotes proliferation, invasion and migration of human hepatocellular carcinoma Hep3b cells","volume":"752","author":"Xie","year":"2021","journal-title":"Exp. Ther. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2427","DOI":"10.1038\/s41598-020-58947-y","article-title":"CNN3 acts as a potential oncogene in cervical cancer by affecting RPLP1 mRNA expression","volume":"10","author":"Xia","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1186\/s12935-018-0658-0","article-title":"RPLP1 promotes tumor metastasis and is associated with a poor prognosis in triple-negative breast cancer patients","volume":"18","author":"He","year":"2018","journal-title":"Cancer Cell Int."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Barnes, D.J., Hookway, E., Athanasou, N., Kashima, T., Oppermann, U., Hughes, S., Swan, D., Lueerssen, D., Anson, J., and Hassan, A.B. (2016). A germline mutation of CDKN2A and a novel RPLP1-C19MC fusion detected in a rare melanotic neuroectodermal tumor of infancy: A case report. BMC Cancer, 16.","DOI":"10.1186\/s12885-016-2669-3"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1007\/s10616-017-0149-5","article-title":"A guide for endometrial cancer cell lines functional assays using the measures of electronic impedence","volume":"70","author":"Kozak","year":"2018","journal-title":"Cytotechnology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.1016\/j.yexcr.2009.02.007","article-title":"E Rplp1 bypasses replicative senescence and contributes to transformation","volume":"315","author":"Kondoh","year":"2009","journal-title":"Exp. Cell Res."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Perucho, L., Artero-Castro, A., Guerrero, S., Ram\u00f3n y Cajal, S., Lleonart, M.E., and Wang, Z.Q. (2014). RPLP1, a crucial ribosomal protein for embryonic development of the nervous system. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0099956"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1499","DOI":"10.1080\/15548627.2015.1063764","article-title":"Disruption of the ribosomal P complex leads to stress-induced autophagy","volume":"11","author":"Feliciano","year":"2015","journal-title":"Autophagy"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e01706","DOI":"10.1128\/JVI.01706-16","article-title":"RPLP1 and RPLP2 are essential flavivirus host proteins that promote early viral protein accumulation","volume":"91","author":"Campos","year":"2017","journal-title":"J. Virol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ishii, K., Washio, T., Uechi, T., Yoshihama, M., Kenmochi, N., and Tomita, M. (2006). Characteristics and clustering of human ribosomal protein genes. BMC Genom., 7.","DOI":"10.1186\/1471-2164-7-37"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Aursnes, I.A., Rishovd, A.L., Karlsen, H.E., and Gj\u00f8en, T. (2011). Validation of reference genes for quantitative RT-qPCR studies of gene expression in Atlantic cod (Gadus morhua l.) during temperature stress. BMC Res. Notes, 4.","DOI":"10.1186\/1756-0500-4-104"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Marques, T.E., de Mendon\u00e7a, L.R., Pereira, M.G., de Andrade, T.G., Garcia-Cairasco, N., Pa\u00e7\u00f3-Larson, M.L., and Gita\u00ed, D.L.G. (2013). Validation of suitable reference genes for expression studies in different pilocarpine-induced models of mesial temporal lobe epilepsy. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0071892"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1111\/andr.12053","article-title":"Effect of ribonucleic acid (RNA) isolation methods on putative reference genes messenger RNA abundance in human spermatozoa","volume":"3","author":"Llonch","year":"2015","journal-title":"Andrology"},{"key":"ref_26","first-page":"3946","article-title":"Selection of reference genes for expression analyses in liver of rats with impaired glucose metabolism","volume":"8","author":"Curi","year":"2015","journal-title":"Int. J. Clin. Exp. Pathol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e02156","DOI":"10.1016\/j.heliyon.2019.e02156","article-title":"Selection of best reference genes for qRT-PCR analysis of human neural stem cells preconditioned with hypoxia or baicalein-enriched fraction extracted from Oroxylum indicum medicinal plant","volume":"5","author":"Kang","year":"2019","journal-title":"Heliyon"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s11010-019-03584-x","article-title":"Selection of optimal reference genes for gene expression studies in chronically hypoxic rat heart","volume":"461","author":"Benak","year":"2019","journal-title":"Mol. Cell Biochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"21711","DOI":"10.1038\/s41598-020-78863-5","article-title":"Analysis of the stability of 70 housekeeping genes during iPS reprogramming","volume":"10","author":"Panina","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1002\/jcp.22440","article-title":"Reprogramming the pluripotent cell cycle: Restoration of an abbreviated G1 phase in human induced pluripotent stem (iPS) cells","volume":"226","author":"Ghule","year":"2011","journal-title":"J. Cell Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.cub.2010.11.049","article-title":"A high proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity","volume":"21","author":"Ruiz","year":"2011","journal-title":"Curr. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1002\/jcp.24104","article-title":"The abbreviated pluripotent cell cycle","volume":"228","author":"Kapinas","year":"2013","journal-title":"J. Cell Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"bbaa389","DOI":"10.1093\/bib\/bbaa389","article-title":"Dynamics of transcriptional and post-transcriptional regulation","volume":"22","author":"Furlan","year":"2021","journal-title":"Brief Bioinform."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1007\/s00018-018-2940-7","article-title":"Regulatory network of miRNA on its target: Coordination between transcriptional and post-transcriptional regulation of gene expression","volume":"76","author":"Pu","year":"2019","journal-title":"Cell Mol. Life. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4738","DOI":"10.12659\/MSM.908812","article-title":"Correlation of MACC1\/c-Myc expression in endometrial carcinoma with clinical\/pathological features or prognosis","volume":"24","author":"Zhang","year":"2018","journal-title":"Med. Sci. Monit."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1016\/0002-9378(91)90580-K","article-title":"c-myc protooncogene polypeptide expression in endometriosis","volume":"164","author":"Schenken","year":"1991","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1016\/j.fertnstert.2012.06.056","article-title":"The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogen-regulated genes implicated in proliferation, is increased in peritoneal endometriosis","volume":"98","author":"Pellegrini","year":"2012","journal-title":"Fertil. Steril."},{"key":"ref_38","first-page":"363","article-title":"Demonstration and biological significance of viral and cellular oncogenes in uterine carcinomas","volume":"75","author":"Wilckens","year":"1991","journal-title":"Verh. Dtsch. Ges. Pathol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1177\/0960327111417266","article-title":"Identification of differentially expressed genes by 2,3,7,8-tetrachlorodibenzo-p-dioxin in human bronchial epithelial cells","volume":"31","author":"Jin","year":"2012","journal-title":"Hum. Exp. Toxicol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1159\/000052859","article-title":"The pathophysiology of endometriosis: Pollution and dioxin","volume":"47","author":"Koninckx","year":"1999","journal-title":"Gynecol. Obstet. Investig."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1093\/toxsci\/70.2.161","article-title":"Environmental dioxins and endometriosis","volume":"70","author":"Rier","year":"2002","journal-title":"Toxicol. Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.reprotox.2016.07.007","article-title":"Exposure to the environmental endocrine disruptor TCDD and human reproductive dysfunction: Translating lessons from murine models","volume":"68","author":"Gnecco","year":"2017","journal-title":"Reprod. Toxicol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1006\/abbi.1999.1288","article-title":"Role of estradiol receptor-\u03b1 in differential expression of 2,3,7,8-tetrachlorodibenzo-p-dioxin-inducible genes in the RL95-2 and KLE human endometrial cancer cell lines","volume":"368","author":"Jana","year":"1999","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1093\/oxfordjournals.aje.a009069","article-title":"Cancer mortality in workers exposed to phenoxy herbicides, chlorophenols, and dioxins. An expanded and updated international cohort study","volume":"145","author":"Kogevinas","year":"1997","journal-title":"Am. J. Epidemol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"S72","DOI":"10.1038\/sj.leu.2401290","article-title":"Dioxin exposure and human leukemias and lymphomas. Lessons from the Seveso accident and studies on industrial workers","volume":"13","author":"Bertazzi","year":"1999","journal-title":"Leukemia"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1093\/humupd\/7.3.331","article-title":"Human health effects of dioxins: Cancer, reproductive and endocrine system effects","volume":"7","author":"Kogevinas","year":"2001","journal-title":"Hum. Reprod. Update"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"hoac009","DOI":"10.1093\/hropen\/hoac009","article-title":"ESHRE guidelines: Endometriosis","volume":"2022","author":"Becker","year":"2022","journal-title":"Hum. Reprod. Open"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.bpobgyn.2018.01.013","article-title":"Ultrasound diagnosis of endometriosis and adenomyosis: State of the art","volume":"51","year":"2018","journal-title":"Best. Prac. Res. Clin. Obstet. Gynecol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/S0002-9378(96)70422-2","article-title":"Management of endometrial cancer","volume":"174","author":"Homesley","year":"1996","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/j.yexcr.2018.06.037","article-title":"Desmoglein 3-influence on oral carcinoma cell migration and invasion","volume":"370","author":"Apu","year":"2018","journal-title":"Exp. Cell Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1038\/s41419-021-04206-5","article-title":"Alpelisib combination treatment as novel targeted therapy against hepatocellular carcinoma","volume":"12","author":"Xu","year":"2021","journal-title":"Cell Death Dis."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/s41419-019-1389-4","article-title":"MEK inhibition suppresses K-Ras wild-type cholangiocarcinoma in vitro and in vivo via inhibiting cell proliferation and modulating tumor microenvironment","volume":"10","author":"Wang","year":"2019","journal-title":"Cell Death Dis."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/3\/2690\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:19:26Z","timestamp":1760120366000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/3\/2690"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,31]]},"references-count":52,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["ijms24032690"],"URL":"https:\/\/doi.org\/10.3390\/ijms24032690","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,31]]}}}