Combined expression levels of KDM2A and KDM2B correlate with nucleolar size and prognosis in primary breast carcinomas.
Biomarkers, Tumor
/ genetics
Breast Neoplasms
/ enzymology
Carcinoma, Ductal, Breast
/ enzymology
Carcinoma, Lobular
/ enzymology
Cell Nucleolus
/ enzymology
F-Box Proteins
/ genetics
Female
Gene Expression Regulation, Neoplastic
Humans
Jumonji Domain-Containing Histone Demethylases
/ genetics
Prognosis
Retrospective Studies
Ribosomes
/ genetics
Journal
Histology and histopathology
ISSN: 1699-5848
Titre abrégé: Histol Histopathol
Pays: Spain
ID NLM: 8609357
Informations de publication
Date de publication:
Oct 2020
Oct 2020
Historique:
pubmed:
10
9
2020
medline:
2
10
2021
entrez:
9
9
2020
Statut:
ppublish
Résumé
Ribosome biogenesis is a fine-tuned cellular process and its deregulation is linked to cancer progression: tumors characterized by an intense ribosome biogenesis often display a more aggressive behavior. Ribosomal RNA (rRNA) synthesis is controlled at several levels, the higher one being the epigenetic regulation of the condensation of chromatin portions containing rRNA genes. KDM2A and KDM2B (Lysine (K)-specific demethylase 2A / B) are histone demethylases modulating the accessibility of ribosomal genes, thereby regulating their transcription. Both enzymes are able to demethylate lysins at relevant sites (e.g. K4, K36) on histone H3. We previously demonstrated that KDM2B is one of the factors regulating ribosome biogenesis in human breast cancer. In this study we aimed to define the combined contribution of KDM2A and KDM2B to breast cancer outcome. KDM2A and KDM2B mRNA levels, nucleolar area as a marker of ribosome biogenesis, and patients' prognosis were retrospectively assessed in a series of primary breast carcinomas. We observed that tumors characterized by reduced levels of both KDM2A and KDM2B displayed a particularly aggressive clinical behavior and increased nucleolar size. Our results suggest that KDM2A and KDM2B may cooperate in regulating ribosome biogenesis thus influencing the biological behavior and clinical outcome of human breast cancers.
Identifiants
pubmed: 32901907
pii: HH-18-248
doi: 10.14670/HH-18-248
doi:
Substances chimiques
Biomarkers, Tumor
0
F-Box Proteins
0
Jumonji Domain-Containing Histone Demethylases
EC 1.14.11.-
KDM2A protein, human
EC 1.14.11.27
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1181-1187Subventions
Organisme : Fondazione AIRC
ID : IG15212
Organisme : Fondazione AIRC
ID : MFAG19941
Références
Ceccarelli C., Trerè D., Santini D., Taffurelli M., Chieco P. and Derenzini M. (2000). AgNORs in breast tumours. Micron 31, 143-149.
pubmed: 10588060
Chen J.Y., Luo C.W., Lai Y.S., Wu C.C. and Hung W.C. (2017). Lysine demethylase KDM2A inhibits TET2 to promote DNA methylation and silencing of tumor suppressor genes in breast cancer. Oncogenesis 6, e369.
pmcid: PMC5608919
pubmed: 28785073
Curigliano G., Burstein H.J., Winer E.P., Gnant M., Dubsky P., Loibl S., Colleoni M,. Regan M.M., Piccart-Gebhart M., Senn H.J., Thürlimann B.; St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2017, André F., Baselga J., Bergh J., Bonnefoi H., Brucker S.Y., Cardoso F., Carey L., Ciruelos E., Cuzick J., Denkert C., Di Leo A., Ejlertsen B., Francis P., Galimberti V., Garber J., Gulluoglu B., Goodwin P., Harbeck N., Hayes D.F., Huang C.S., Huober J., Hussein K., Jassem J., Jiang Z., Karlsson P., Morrow M., Orecchia R., Osborne K.C., Pagani O., Partridge A.H., Pritchard K., Ro J., Rutgers E.J.T., Sedlmayer F., Semiglazov V., Shao Z., Smith I., Toi M., Tutt A., Viale G., Watanabe T., Whelan T.J. and Xu B. (2017). De-escalating and escalating treatments for early-stage breast cancer: The St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017. Ann. Oncol. 28, 1700-1712.
pmcid: PMC6246241
pubmed: 28838210
Derenzini M., Montanaro L. and Treré D. (2009). What the nucleolus says to a tumour pathologist. Histopathology 54, 753-762.
pubmed: 19178588
Dussault A.A. and Pouliot M. (2006). Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol. Proced. Online 8, 1-10.
pmcid: PMC1352391
pubmed: 16446781
Frescas D., Guardavaccaro D., Bassermann F., Koyama-Nasu R. and Pagano M. (2007). JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes. Nature 450, 309- 313.
pubmed: 17994099
Galbiati A., Penzo M., Bacalini M.G., Onofrillo C., Guerrieri A.N., Garagnani P., Franceschi C., Treré D. and Montanaro L. (2017). Epigenetic up-regulation of ribosome biogenesis and more aggressive phenotype triggered by the lack of the histone demethylase JHDM1B in mammary epithelial cells. Oncotarget 8, 37091-37103.
pmcid: PMC5514893
pubmed: 28415746
Grummt I. and Längst G. (2013). Epigenetic control of RNA polymerase I transcription in mamma-lian cells. Biochim. Biophys. Acta 1829, 393-404.
pubmed: 23063748
Hernandez-Verdun D. (2006). Nucleolus: From structure to dynamics. Histochem. Cell Biol. 125, 127-137.
pubmed: 16328431
Kopp K., Gasiorowski J.Z., Chen D., Gilmore R., Norton J.T., Wang C., Leary D.J., Chan E.K.L., Dean D.A. and Huang S. (2007). Pol I transcription and pre-rRNA processing are coordinated in a transcription-dependent manner in mammalian cells. Mol. Biol. Cell 18, 394-403.
pmcid: PMC1783775
pubmed: 17108330
Kressler D., Hurt E. and Baßler J. (2010). Driving ribosome assembly. Biochim. Biophys. Acta 1803, 673-683.
pubmed: Kressler D., Hurt E. and Baßler J. (2010). Driving ribosome assembly.
Biochim. Biophys. Acta 1803, 673-683.
Lawrence R.J., Earley K., Pontes O., Silva M., Chen Z.J., Neves N., Viegas W. and Pikaard C.S. (2004). A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cell 13, 599-609
pubmed: 14992728
Lempiäinen H. and Shore D. (2009). Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 21, 855-863
pubmed: 19796927
Martin C. and Zhang Y. (2005). The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 855-863.
pubmed: 16261189
Montanaro L., Brigotti M., Clohessy J., Barbieri S., Ceccarelli C., Santini D., Taffurelli M., Calienni M., Teruya-Feldstien J., Trerè D., Pandolfi P.P. and Derenzini M. (2006). Dyskerin expression influences the level of ribosomal RNA pseudo-uridylation and telomerase RNA component in hu-man breast cancer. J. Pathol. 210, 10-18.
pubmed: 16841302
Montanaro L., Treré D. and Derenzini M. (2008). Nucleolus, ribosomes, and cancer. Am. J. Pathol. 173, 301-310
pmcid: PMC2475768
pubmed: 18583314
Montanaro L., Treré D. and Derenzini M. (2013). The emerging role of RNA polymerase I tran-scription machinery in human malignancy: A clinical perspective. Onco Targets Ther. 6, 909-916.
pmcid: PMC3722134
pubmed: 23888116
Pan D., Mao C., Zou T., Yao A.Y., Cooper M.P., Boyartchuk V. and Wang Y.X. (2012). The histone demethylase Jhdm1a regulates hepatic gluconeogenesis. PLoS Genet. 8, e1002761.
pmcid: PMC3375226
pubmed: 22719268
Penzo M., Casoli L., Pollutri D., Sicuro L., Ceccarelli C., Santini D., Taffurelli M., Govoni M., Brina D., Trerè D. and Montanaro L. (2015). JHDM1B expression regulates ribosome biogenesis and cancer cell growth in a p53 dependent manner. Int. J. Cancer 136, E272-E281.
pubmed: 25273595
Penzo M., Montanaro L., Treré D. and Derenzini M. (2019). The ribosome biogenesis—Cancer connection. Cells 8, 55.
pmcid: PMC6356843
pubmed: 30650663
Ploton D., Menager M., Jeannesson P., Himber G., Pigeon F. and Adnet J.J. (1986). Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level. Histochem. J. 18, 5-14.
pubmed: 2423479
Rizwani W., Schaal C., Kunigal S., Coppola D. and Chellappan S. (2014). Mammalian lysine histone demethylase KDM2A regulates E2F1-mediated gene transcription in breast cancer cells. PLoS One 9, e100888
pmcid: PMC4100745
pubmed: 25029110
Sirri V., Roussel P. and Hernandez-Verdun D. (2000). The AgNOR proteins: Qualitative and quan-titative changes during the cell cycle. Micron 31, 121-126.
pubmed: 10588057
Tanaka Y., Okamoto K., Teye K., Umata T., Yamagiwa N., Suto Y., Zhang Y. and Tsuneoka M. (2010). JmjC enzyme KDM2A is a regulator of rRNA transcription in response to starvation. EMBO J. 29, 1510-1522.
pmcid: PMC2876952
pubmed: 20379134
Tanaka Y., Yano H., Ogasawara S., Yoshioka S., Imamura H., Okamoto K. and Tsuneoka M. (2015). Mild glucose starvation induces KDM2A-mediated H3K36me2 demethylation through AMPK to reduce rRNA transcription and cell proliferation. Mol. Cell. Biol. 35, 4170-4184.
pmcid: PMC4648824
pubmed: 26416883
Thomson E., Ferreira-Cerca S. and Hurt E. (2013). Eukaryotic ribosome biogenesis at a glance. J. Cell Sci. 126, 4815-4821.
pubmed: 24172536
Tsukada Y.I., Fang J., Erdjument-Bromage H., Warren M.E., Borchers C.H., Tempst P. and Zhang Y. (2006). Histone demethylation by a family of JmjC domain-containing proteins. Nature 439, 811- 816.
pubmed: 16362057
Xu W.H., Liang D.Y., Wang Q., Shen J., Liu Q.H. and Peng Y.B. (2019). Knockdown of KDM2A inhibits proliferation associated with TGF-β expression in HEK293T cell. Mol. Cell Biochem. 6, 838-849
pubmed: 30604066
Yan W., Herman J.G. and Guo M. (2016). Epigenome-based personalized medicine in human cancer. Epigenomics 8, 119-133.
pubmed: 26344672