Modulation of estrogenic action in clear cell carcinoma of the ovary (Review)

Tanase,Yasuhito; Yamada,Yoshihiko; Shigetomi,Hiroshi; Kajihara,Hirotaka; Oonogi,Akira; Yoshizawa,Yoriko; Furukawa,Naoto; Haruta,Shoji; Yoshida,Shozo; Sado,Toshiyuki; Oi,Hidekazu; Kobayashi,Hiroshi

doi:10.3892/etm.2011.376

Modulation of estrogenic action in clear cell carcinoma of the ovary (Review)

Authors:
- Yasuhito Tanase
- Yoshihiko Yamada
- Hiroshi Shigetomi
- Hirotaka Kajihara
- Akira Oonogi
- Yoriko Yoshizawa
- Naoto Furukawa
- Shoji Haruta
- Shozo Yoshida
- Toshiyuki Sado
- Hidekazu Oi
- Hiroshi Kobayashi
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Affiliations: Department of Obstetrics and Gynecology, Nara Medical University, Nara, Japan
Published online on: October 24, 2011 https://doi.org/10.3892/etm.2011.376
Pages: 18-24

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Abstract

Two histologic types, clear cell carcinoma (CCC) and endometrioid adenocarcinoma (EAC), are the common histology in ovarian cancer patients who have associated endometriosis. However, both tumor types have distinct clinicopathological characteristics and molecular phenotypes. EAC is predominantly positive for estrogen receptor (ER), but CCC specifically exhibits lower ER expression. This study reviews the current understanding of the role of the ER information in the pathogenesis of CCC, as well as the English language literature for biochemical studies on ER expression and estrogenic action in CCC. The iron-mediated oxidative stress occurs due to repeated hemorrhage in endometriosis, then this compound oxidatively modifies genomic DNA and, subsequently, ER depletion may be observed. There are a number of factors that interfere with ER expression and estrogen activity, which include DNA methylation of the promoter region, histone deacetylation, heme and iron binding, chromatin remodeling and ubiquitin ligase activity. Loss of estrogen function may be a turning point in CCC progression and aggressiveness.

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1.	M TakanoY KikuchiN YaegashiK KuzuyaM UekiH TsudaM SuzukiJ KigawaS TakeuchiH TsudaT MoriyaT SugiyamaClear cell carcinoma of the ovary: a retrospective multicentre experience of 254 patients with complete surgical stagingBr J Cancer9413691374200610.1038/sj.bjc.660311616641903
2.	T KitaY KikuchiK KudohM TakanoT GotoJ HirataT TodeI NagataExploratory study of effective chemotherapy to clear cell carcinoma of the ovaryOncol Rep7327331200010671681
3.	DA BellOrigins and molecular pathology of ovarian cancerMod Pathol18S19S32200510.1038/modpathol.380030615761464
4.	M MandaiK YamaguchiN MatsumuraT BabaI KonishiOvarian cancer in endometriosis: molecular biology, pathology, and clinical managementInt J Clin Oncol14383391200910.1007/s10147-009-0935-y19856044
5.	H KobayashiOvarian cancer in endometriosis: epidemiology, natural history, and clinical diagnosisInt J Clin Oncol14378382200910.1007/s10147-009-0931-219856043
6.	DM DinulescuTA InceBJ QuadeSA ShaferD CrowleyT JacksRole of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancerNat Med116370200510.1038/nm117315619626
7.	H KobayashiY YamadaS KanayamaN FurukawaT NoguchiS HarutaS YoshidaM SakataT SadoH OiThe role of hepatocyte nuclear factor-1beta in the pathogenesis of clear cell carcinoma of the ovaryInt J Gynecol Cancer19471479200910.1111/IGC.0b013e3181a19eca19407577
8.	K YamaguchiM MandaiS ToyokuniJ HamanishiT HiguchiK TakakuraS FujiiContents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stressClin Cancer Res143240200810.1158/1078-0432.CCR-07-161418172249
9.	K YamaguchiM MandaiT OuraN MatsumuraJ HamanishiT BabaS MatsuiSK MurphyI KonishiIdentification of an ovarian clear cell carcinoma gene signature that reflects inherent disease biology and the carcinogenic processesOncogene2917411752201010.1038/onc.2009.47020062075
10.	H KobayashiH KajiwaraS KanayamaY YamadaN FurukawaT NoguchiS HarutaS YoshidaM SakataT SadoH OiMolecular pathogenesis of endometriosis-associated clear cell carcinoma of the ovary (Review)Oncol Rep22233240200919578761
11.	S YoshidaN FurukawaS HarutaY TanaseS KanayamaT NoguchiM SakataY YamadaH OiH KobayashiTheoretical model of treatment strategies for clear cell carcinoma of the ovary: focus on perspectivesCancer Treat Rev35608615200910.1016/j.ctrv.2009.07.00219665848
12.	KK ChanN WeiSS LiuL Xiao-YunAN CheungHY NganEstrogen receptor subtypes in ovarian cancer: a clinical correlationObstet Gynecol111144151200810.1097/01.AOG.0000296715.07705.e918165403
13.	C ZamagniRM WirtzP de IacoM RosatiE VeltrupF RosatiE CapizziN CacciariC AlboniA BernardiF MassariS QuerciaA D'Errico GrigioniM DietelJ SehouliC DenkertAA MartoniOestrogen receptor 1 mRNA is a prognostic factor in ovarian cancer patients treated with neo-adjuvant chemotherapy: determination by array and kinetic PCR in fresh tissue biopsiesEndocr Relat Cancer1612411249200910.1677/ERC-08-0342
14.	RA SoslowHistologic subtypes of ovarian carcinoma: an overviewInt J Gynecol Pathol27161174200818317227
15.	F SuzukiJ AkahiraI MiuraT SuzukiK ItoS HayashiH SasanoN YaegashiLoss of estrogen receptor beta isoform expression and its correlation with aberrant DNA methylation of the 5′-untranslated region in human epithelial ovarian carcinomaCancer Sci9923652372200819032364
16.	E SwedenborgKA PowerW CaiI PongratzJ RüeggRegulation of estrogen receptor beta activity and implications in health and diseaseCell Mol Life Sci6638733894200910.1007/s00018-009-0118-z19669093
17.	SH KaoHC HuangRH HsiehSC ChenMC TsaiCR TzengOxidative damage and mitochondrial DNA mutations with endometriosisAnn NY Acad Sci1042186194200510.1196/annals.1338.02115965062
18.	LS KristensenHM NielsenLL HansenEpigenetics and cancer treatmentEur J Pharmacol625131142200910.1016/j.ejphar.2009.10.01119836388
19.	KV DonkenaCY YoungDJ TindallOxidative stress and DNA methylation in prostate cancerObstet Gynecol IntJune2010(E-pub ahead of print).
20.	YL OttavianoJP IssaFF ParlHS SmithSB BaylinNE DavidsonMethylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cellsCancer Res542552255519948168078
21.	L GiacintiPP ClaudioM LopezA GiordanoEpigenetic information and estrogen receptor alpha expression in breast cancerOncologist1118200610.1634/theoncologist.11-1-116401708
22.	C DannenmannN ShabaniK FrieseU JeschkeI MylonasA BrüningThe metastasis-associated gene MTA1 is upregulated in advanced ovarian cancer, represses ERbeta, and enhances expression of oncogenic cytokine GROCancer Biol Ther714601467200810.4161/cbt.7.9.642718719363
23.	D ConteS NarindrasorasakB SarkarIn vivo and in vitro iron-replaced zinc finger generates free radicals and causes DNA damageJ Biol Chem27151255130199610.1074/jbc.271.9.51258617792
24.	S RaghuramKR StayrookP HuangPM RogersAK NosieDB McClureLL BurrisS KhorasanizadehTP BurrisF RastinejadIdentification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbetaNat Struct Mol Biol1412071213200710.1038/nsmb134418037887
25.	MC SugdenMJ HolnessRole of nuclear receptors in the modulation of insulin secretion in lipid-induced insulin resistanceBiochem Soc Trans36891900200810.1042/BST036089118793157
26.	J HuuskonenM VishnuPE FieldingCJ FieldingActivation of ATP-binding cassette transporter A1 transcription by chromatin remodeling complexArterioscler Thromb Vasc Biol2511801185200510.1161/01.ATV.0000163186.58462.c515774904
27.	XS LiP TrojerT MatsumuraJE TreismanN TaneseMammalian SWI/SNF – a subunit BAF250/ARID1 is an E3 ubiquitin ligase that targets histone H2BMol Cell Biol30167316882010
28.	KC WiegandSP ShahOM Al-AghaARID1A mutations in endometriosis-associated ovarian carcinomasN Engl J Med36315321543201010.1056/NEJMoa100843320942669
29.	S JonesTL WangIeM ShihTL MaoK NakayamaR RodenR GlasD SlamonLA Diaz JrB VogelsteinKW KinzlerVE VelculescuN PapadopoulosFrequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinomaScience330228231201010.1126/science.119633320826764
30.	T OhtaM FukudaUbiquitin and breast cancerOncogene2320792088200410.1038/sj.onc.120737115021895
31.	H ItamochiJ KigawaN TerakawaMechanisms of chemoresistance and poor prognosis in ovarian clear cell carcinomaCancer Sci99653658200810.1111/j.1349-7006.2008.00747.x18377417
32.	H KajiharaY YamadaS KanayamaN FurukawaT NoguchiS HarutaS YoshidaT SadoH OiH KobayashiClear cell carcinoma of the ovary: potential pathogenic mechanisms (Review)Oncol Rep2311931203201020372830
33.	A TsuchiyaM SakamotoJ YasudaM ChumaT OhtaM OhkiT YasugiY TaketaniS HirohashiExpression profiling in ovarian clear cell carcinoma: identification of hepatocyte nuclear factor-1 beta as a molecular marker and a possible molecular target for therapy of ovarian clear cell carcinomaAm J Pathol16325032512200310.1016/S0002-9440(10)63605-X
34.	N KatoG TamuraT MotoyamaHypomethylation of hepatocyte nuclear factor-1beta (HNF-1beta) CpG island in clear cell carcinoma of the ovaryVirchows Arch452175180200810.1007/s00428-007-0543-z18066692
35.	N KatoS SasouT MotoyamaExpression of hepatocyte nuclear factor-1beta (HNF-1beta) in clear cell tumors and endometriosis of the ovaryMod Pathol198389200610.1038/modpathol.380049216258507
36.	N KatoM ToukairinI AsanumaT MotoyamaImmunocytochemistry for hepatocyte nuclear factor-1beta (HNF-1beta): a marker for ovarian clear cell carcinomaDiagn Cytopathol35193197200710.1002/dc.2062317351940
37.	N KatoT MotoyamaHepatocyte nuclear factor-1beta (HNF-1beta) in human urogenital organs: its expression and role in embryogenesis and tumorigenesisHistol Histopathol2414791486200919760597
38.	S YamamotoH TsudaS AidaH ShimazakiS TamaiO MatsubaraImmunohistochemical detection of hepatocyte nuclear factor 1beta in ovarian and endometrial clear-cell adenocarcinomas and nonneoplastic endometriumHum Pathol3810741080200710.1016/j.humpath.2006.12.01817442376
39.	MJ BirrerThe origin of ovarian cancer – is it getting clearer?N Engl J Med363157415752010