The epigenetic EZH2/H3K27me3 axis modulates lactotroph tumor cell proliferation

in Journal of Endocrinology
Authors:
N Zlocowski Centro de Microscopía Electrónica, Facultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, ArgentinaFacultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina

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https://orcid.org/0000-0003-0268-9342
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L d V Sosa Centro de Microscopía Electrónica, Facultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, ArgentinaFacultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina

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B De la Cruz-Thea Cellular and Molecular Neurobiology Department, CONICET - Universidad Nacional de Córdoba - Instituto de Investigación Médica Mercedes y Martín Ferreyra, Córdoba, Argentina

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C B Guido Centro de Microscopía Electrónica, Facultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, ArgentinaFacultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina

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M G Martín Cellular and Molecular Neurobiology Department, CONICET - Universidad Nacional de Córdoba - Instituto de Investigación Médica Mercedes y Martín Ferreyra, Córdoba, Argentina

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J H Mukdsi Centro de Microscopía Electrónica, Facultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, ArgentinaFacultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina

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A I Torres Centro de Microscopía Electrónica, Facultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, ArgentinaFacultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina

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J P Petiti Centro de Microscopía Electrónica, Facultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, ArgentinaFacultad de Ciencias Médicas (CME-FCM) - Instituto de Investigaciones en Ciencias de la Salud, Consejo Nacional de Investigaciones Científicas Técnicas (INICSA-CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina

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Correspondence should be addressed to J Petiti: jpetiti@cmefcm.uncor.edu
DOI:
https://doi.org/10.1530/JOE-22-0195
Volume/Issue:
Volume 257: Issue 2
Article Type:
Research Article
Article ID:
e220195
Online Publication Date:
30 Mar 2023
Copyright:
© Society for Endocrinology 2023
Restricted access
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Interest in epigenetics has gained substantial momentum as a result of their identified role in the regulation of tumor progression as well as their ability to pharmacologically target genes. Pituitary neuroendocrine tumors (PitNETs) tend to be inactivated via epigenetic modification, and although emerging evidence has suggested a role for epigenetic factors in PitNET tumorigenesis, the degree to which these factors may be targeted by new therapeutic strategies still remains poorly understood. The objective of the present study was to examine the participation of the EZH2/H3K27me3 axis in the proliferation of lactotroph tumor cells. We demonstrated that the levels of EZH2 and H3K27me3 were increased in murine experimental prolactin (PRL) tumors with respect to a control pituitary, in contrast with the low p21 mRNA levels encountered, with an H3K27me3 enrichment being observed in its promoter region in a GH3 tumor cell. Furthermore, specific EZH2/H3K27me3 axis inhibition blocked the proliferation of primary tumor cell culture and GH3 cells, thereby making it an attractive therapeutic target for PRL PitNETs.

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Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© Society for Endocrinology 2023
Article ID:
e220195
Article Type:
Research Article
Received Date:
17 Jan 2023
Accepted Date:
10 Feb 2023
Print Publication Date:
01 May 2023
Online Publication Date:
30 Mar 2023
Keywords:
H3K27me3; EZH2; GSK343; PRL tumor

  • Albert M & Helin K 2010 Histone methyltransferases in cancer. Seminars in Cell and Developmental Biology 21 209–220. (https://doi.org/10.1016/j.semcdb.2009.10.007)

  • Asa SL 2008 Practical pituitary pathology: what does the pathologist need to know? Archives of Pathology and Laboratory Medicine 132 1231–1240. (https://doi.org/10.5858/2008-132-1231-PPPWDT)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Asa SL, Casar-Borota O, Chanson P, Delgrange E, Earls P, Ezzat S, Grossman A, Ikeda H, Inoshita N & Karavitaki N et al.2017 From pituitary adenoma to pituitary neuroendocrine tumor (PitNET): an International Pituitary Pathology Club proposal. Endocrine-Related Cancer 24 C5–C8. (https://doi.org/10.1530/ERC-17-0004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Asa SL & Ezzat S 2002 The pathogenesis of pituitary tumours. Nature Reviews. Cancer 2 836–849. (https://doi.org/10.1038/nrc926)

  • Asa SL, Mete O & Ezzat S 2021 Genomics and epigenomics of pituitary tumors: what do pathologists need to know? Endocrine Pathology 32 3–16. (https://doi.org/10.1007/s12022-021-09663-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bownesv LV, Williams AP, Marayati R, Stafman LL, Markert H, Quinn CH, Wadhwani N, Aye JM, Stewart JE & Yoon KJ et al.2021 EZH2 inhibition decreases neuroblastoma proliferation and in vivo tumor growth. PLoS One 16 e0246244. (https://doi.org/10.1371/journal.pone.0246244)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chang M, Yang C, Bao X & Wang R 2020 Genetic and epigenetic causes of pituitary adenomas. Frontiers in Endocrinology 11 596554. (https://doi.org/10.3389/fendo.2020.596554)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chen Q, Zheng PS & Yang WT 2016 EZH2-mediated repression of GSK-3beta and TP53 promotes Wnt/beta-catenin signaling-dependent cell expansion in cervical carcinoma. Oncotarget 7 36115–36129. (https://doi.org/10.18632/oncotarget.8741)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • D’Amico F & Skarmoutsou E 2008 Quantifying immunogold labelling in transmission electron microscopy. Journal of Microscopy 230 9–15. (https://doi.org/10.1111/j.1365-2818.2008.01949.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dai C, Kang J, Liu X, Yao Y, Wang H & Wang R 2021 How to classify and define pituitary tumors: recent advances and current controversies. Frontiers in Endocrinology 12 604644. (https://doi.org/10.3389/fendo.2021.604644)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • de Paul AL, Pons P, Aoki A & Torres AI 1997 Heterogeneity of pituitary lactotrophs: immunocytochemical identification of functional subtypes. Acta Histochemica 99 277–289. (https://doi.org/10.1016/S0065-1281(9780022-0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Deb G, Singh AK & Gupta S 2014 EZH2: not EZHY (easy) to deal. Molecular Cancer Research 12 639–653. (https://doi.org/10.1158/1541-7786.MCR-13-0546)

  • Dong W, Li J, Liu Q, Liu C, Li C, Song G, Zhu H, Gao H & Zhang Y 2018 P21(Waf1/Cip1) and p27(Kip1) are correlated with the development and invasion of prolactinoma. Journal of Neuro-Oncology 136 485–494. (https://doi.org/10.1007/s11060-017-2683-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Duan R, Du W & Guo W 2020 EZH2: a novel target for cancer treatment. Journal of Hematology and Oncology 13 104. (https://doi.org/10.1186/s13045-020-00937-8)

  • Dworakowska D & Grossman AB 2018 Aggressive and malignant pituitary tumours: state-of-the-art. Endocrine-Related Cancer 25 R559–R575. (https://doi.org/10.1530/ERC-18-0228)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ebrahimi A, Schittenhelm J, Honegger J & Schluesener HJ 2011 Histone acetylation patterns of typical and atypical pituitary adenomas indicate epigenetic shift of these tumours. Journal of Neuroendocrinology 23 525–530. (https://doi.org/10.1111/j.1365-2826.2011.02129.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Eich ML, Athar M, Ferguson JE 3rd & Varambally S 2020 EZH2-targeted therapies in cancer: hype or a reality. Cancer Research 80 5449–5458. (https://doi.org/10.1158/0008-5472.CAN-20-2147)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Eljarmak D, Lis M, Cantin M, Carrière PD & Collu R 1985 Effects of chronic bromocriptine treatment of an estrone-induced, prolactin-secreting rat pituitary adenoma. Hormone Research 21 160–167. (https://doi.org/10.1159/000180041)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ezzat S, Cheng S & Asa SL 2018 Epigenetics of pituitary tumors: pathogenetic and therapeutic implications. Molecular and Cellular Endocrinology 469 70–76. (https://doi.org/10.1016/j.mce.2017.07.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Farrell WE 2014 Epigenetics of pituitary tumours: an update. Current Opinion in Endocrinology, Diabetes, and Obesity 21 299–305. (https://doi.org/10.1097/MED.0000000000000078)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ferraris J, Zárate S, Jaita G, Boutillon F, Bernadet M, Auffret J, Seilicovich A, Binart N, Goffin V & Pisera D 2014 Prolactin induces apoptosis of lactotropes in female rodents. PLoS One 9 e97383. (https://doi.org/10.1371/journal.pone.0097383)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Filippakopoulos P & Knapp S 2014 Targeting bromodomains: epigenetic readers of lysine acetylation. Nature Reviews. Drug Discovery 13 337–356. (https://doi.org/10.1038/nrd4286)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Guido CB, Sosa LDV, Perez PA, Zlocoswki N, Velazquez FN, Gutierrez S, Petiti JP, Mukdsi JH & Torres AI 2021 Changes of stem cell niche during experimental pituitary tumor development. Journal of Neuroendocrinology 33 e13051. (https://doi.org/10.1111/jne.13051)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hauser BM, Lau A, Gupta S, Bi WL & Dunn IF 2019 The epigenomics of pituitary adenoma. Frontiers in Endocrinology (Lausanne) 10 290. (https://doi.org/10.3389/fendo.2019.00290)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heaney AP, Horwitz GA, Wang Z, Singson R & Melmed S 1999 Early involvement of estrogen-induced pituitary tumor transforming gene and fibroblast growth factor expression in prolactinoma pathogenesis. Nature Medicine 5 1317–1321. (https://doi.org/10.1038/15275)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jackson JP, Lindroth AM, Cao X & Jacobsen SE 2002 Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416 556–560. (https://doi.org/10.1038/nature731)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jones BA, Varambally S & Arend RC 2018 Histone methyltransferase EZH2: A therapeutic target for ovarian cancer. Molecular Cancer Therapeutics 17 591–602. (https://doi.org/10.1158/1535-7163.MCT-17-0437)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jung YS, Qian Y & Chen X 2010 Examination of the expanding pathways for the regulation of p21 expression and activity. Cellular Signalling 22 1003–1012. (https://doi.org/10.1016/j.cellsig.2010.01.013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kim KH & Roberts CW 2016 Targeting EZH2 in cancer. Nature Medicine 22 128–134. (https://doi.org/10.1038/nm.4036)

  • Lee JS, Smith E & Shilatifard A 2010 The language of histone crosstalk. Cell 142 682–685. (https://doi.org/10.1016/j.cell.2010.08.011)

  • Li Y, Chen X & Lu C 2021 The interplay between DNA and histone methylation: molecular mechanisms and disease implications. EMBO Reports 22 e51803. (https://doi.org/10.15252/embr.202051803)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu B, Pang B, Wang Q, Yang S, Gao T, Ding Q, Liu H, Yang Y, Fan H & Zhang R et al.2017a EZH2 upregulation correlates with tumor invasiveness, proliferation, and angiogenesis in human pituitary adenomas. Human Pathology 66 101–107. (https://doi.org/10.1016/j.humpath.2017.03.028)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu L, Xu F, Chang CK, He Q, Wu LY, Zhang Z & Li X 2017b MYCN contributes to the malignant characteristics of erythroleukemia through EZH2-mediated epigenetic repression of p21. Cell Death and Disease 8 e3126. (https://doi.org/10.1038/cddis.2017.526)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mehta GU & Jane JAJ 2012 Pituitary tumors. Current Opinion in Neurology 25 751–755. (https://doi.org/10.1097/WCO.0b013e3283587bed)

  • Melmed S 2020 Pituitary-tumor endocrinopathies. New England Journal of Medicine 382 937–950. (https://doi.org/10.1056/NEJMra1810772)

  • Millanes-Romero A, Herranz N, Perrera V, Iturbide A, Loubat-Casanovas J, Gil J, Jenuwein T, García de Herreros A & Peiró S 2013 Regulation of heterochromatin transcription by Snail1/LOXL2 during epithelial-to-mesenchymal transition. Molecular Cell 52 746–757. (https://doi.org/10.1016/j.molcel.2013.10.015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miranda Furtado CL, dos Santos Luciano MC & Santos S 2019. Epidrugs: targeting epigenetic marks in cancer treatment. Epigenetics 14 1164–1176. (https://doi.org/10.1080/15592294.2019.1640546)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mu X, Chen M, Xiao B, Yang B, Singh S & Zhang B 2019 EZH2 confers sensitivity of breast cancer cells to Taxol by attenuating p21 expression epigenetically. DNA and Cell Biology 38 651–659. (https://doi.org/10.1089/dna.2019.4699)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mukdsi JH, de Paul AL, Petiti JP, Gutiérrez S, Aoki A & Torres AI 2006 Pattern of FGF-2 isoform expression correlated with its biological action in experimental prolactinomas. Acta Neuropathologica 112 491–501. (https://doi.org/10.1007/s00401-006-0101-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Neou M, Villa C, Armignacco R, Jouinot A, Raffin-Sanson ML, Septier A, Letourneur F, Diry S, Diedisheim M & Izac B et al.2020 Pangenomic classification of pituitary neuroendocrine tumors. Cancer Cell 37 123–134.e5. (https://doi.org/10.1016/j.ccell.2019.11.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ocker M, Bitar SA, Monteiro AC, Gali-Muhtasib H & & Schneider-Stock R 2019 Epigenetic regulation of p21(cip1/waf1) in human cancer. Cancers (Basel) 11 1343. (https://doi.org/10.3390/cancers11091343)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ohuchi M, Sakamoto Y, Tokunaga R, Kiyozumi Y, Nakamura K, Izumi D, Kosumi K, Harada K, Kurashige J & Iwatsuki M et al.2018 Increased EZH2 expression during the adenoma-carcinoma sequence in colorectal cancer. Oncology Letters 16 5275–5281. (https://doi.org/10.3892/ol.2018.9240)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Otto CA, Marshall JC, Lloydv RV, Sherman PS, Fisher SJ, Valoppi VL, Rogers WL & Wieland DM 1986 Use of DES-treated rats as an animal model for assessment of pituitary adenoma imaging agents. International Journal of Radiation Applications and Instrumentation. Part B, Nuclear Medicine and Biology 13 539–547. (https://doi.org/10.1016/0883-2897(8690135-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Palomer E, Carretero J, Benvegnù S, Dotti CG & Martin MG 2016 Neuronal activity controls bdnf expression via Polycomb de-repression and CREB/CBP/JMJD3 activation in mature neurons. Nature Communications 7 11081. (https://doi.org/10.1038/ncomms11081)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pawlyn C, Bright MD, Buros AF, Stein CK, Walters Z, Aronson LI, Mirabella F, Jones JR, Kaiser MF & Walker BA et al.2017 Overexpression of EZH2 in multiple myeloma is associated with poor prognosis and dysregulation of cell cycle control. Blood Cancer Journal 7 e549. (https://doi.org/10.1038/bcj.2017.27)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sabatino ME, Grondona E & de Paul AL 2022 Architects of pituitary tumour growth. Frontiers in Endocrinology 13 924942. (https://doi.org/10.3389/fendo.2022.924942)

  • Sahores A, Luque GM, Wargon V, May M, Molinolo A, Becu-Villalobos D, Lanari C & Lamb CA 2013 Novel, low cost, highly effective, handmade steroid pellets for experimental studies. PLoS One 8 e64049. (https://doi.org/10.1371/journal.pone.0064049)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schult D, Holsken A, Siegel S, Buchfelder M, Fahlbusch R, Kreitschmann-Andermahr I & Buslei R 2015 EZH2 is highly expressed in pituitary adenomas and associated with proliferation. Scientific Reports 5 16965. (https://doi.org/10.1038/srep16965)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Srirangam Nadhamuni V & Korbonits M 2020 Novel insights into pituitary tumorigenesis: genetic and epigenetic mechanisms. Endocrine Reviews 41 821–846. (https://doi.org/10.1210/endrev/bnaa006)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Stark GR, Wang Y & Lu T 2011 Lysine methylation of promoter-bound transcription factors and relevance to cancer. Cell Research 21 375–380. (https://doi.org/10.1038/cr.2010.174)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Välimäki N, Schalin-Jäntti C, Karppinen A, Paetau A, Kivipelto L, Aaltonen LA & Karhu A 2019 Genetic and epigenetic characterization of growth hormone-secreting pituitary tumors. Molecular Cancer Research: MCR 17 2432–2443. (https://doi.org/10.1158/1541-7786.MCR-19-0434)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RGAB & Otte AP et al.2002 The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419 624–629. (https://doi.org/10.1038/nature01075)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Volkel P, Dupret B, le Bourhis X & Angrand PO 2015 Diverse involvement of EZH2 in cancer epigenetics. American Journal of Translational Research 7 175–193.

  • Xu H, Zhang L, Qian X, Zhou X, Yan Y, Zhou J, Ge W, Albahde M & Wang W 2019 GSK343 induces autophagy and downregulates the AKT/mTOR signaling pathway in pancreatic cancer cells. Experimental and Therapeutic Medicine 18 2608–2616. (https://doi.org/10.3892/etm.2019.7845)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Xu RK, Wu XM, Di AK, Xu JN, Pang CS & Pang SF 2000 Pituitary prolactin-secreting tumor formation: recent developments. Biological Signals and Receptors 9 1–20. (https://doi.org/10.1159/000014618)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yu T, Wang Y, Hu Q, Wu W, Wu Y, Wei W, Han D, You Y, Lin N & Liu N 2017 The EZH2 inhibitor GSK343 suppresses cancer stem-like phenotypes and reverses mesenchymal transition in glioma cells. Oncotarget 8 98348–98359. (https://doi.org/10.18632/oncotarget.21311)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang L, Lu Q & Chang C 2020 Epigenetics in health and disease. Advances in Experimental Medicine and Biology 1253 3–55. (https://doi.org/10.1007/978-981-15-3449-2_1)

  • Zhang Y, Sun Z, Jia J, Du T, Zhang N, Tang Y, Fang Y & Fang D 2021 Overview of histone modification. Advances in Experimental Medicine and Biology 1283 1–16. (https://doi.org/10.1007/978-981-15-8104-5_1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhu X, Lee K, Asa SL & Ezzat S 2007 Epigenetic silencing through DNA and histone methylation of fibroblast growth factor receptor 2 in neoplastic pituitary cells. American Journal of Pathology 170 1618–1628. (https://doi.org/10.2353/ajpath.2007.061111)

    • PubMed
    • Search Google Scholar
    • Export Citation