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High Expression of EZH2 As a Marker for the Differential Diagnosis Of www.nature.com/scientificreports OPEN High expression of EZH2 as a marker for the diferential diagnosis of malignant and benign myogenic Received: 8 November 2017 Accepted: 3 August 2018 tumors Published: xx xx xxxx Ning Zhang1, Zhi Zeng2, Shaobo Li3, Fei Wang4 & Peng Huang5 Overlap in morphologic features between malignant and benign myogenic tumors, such as leiomyosarcoma (LMS) vs. leiomyoma as well as rhabdomyosarcoma (RMS) vs. rhabdomyoma, often makes diferential diagnosis difcult and challenging. Here the expressions of Enhancer of Zeste Homolog 2 (EZH2), Suppressor of Zeste 12 (SUZ12), retinoblastoma protein associated protein 46 (RbAp46), Embryonic Ectoderm Development (EED) and ki-67 protein were detected by immunohistochemistry to evaluate their values in diferential diagnosis. The expression of EZH2 mRNA was investigated by analyzing the Gene Expression Omnibus Datasets. The results demonstrated that EZH2 protein was detected in 81.25% (26/32) of LMS and 70.58% (36/51) of RMS, whereas none of leiomyoma (n = 16), rhabdomyoma (n = 15) and normal tissues (n = 31) showed positive immunostaining (p < 0.05). EZH2 protein was found to have a sensitivity of 91.30% and specifcity of 100% in distinguishing well-diferentiated LMS from cellular leiomyoma, and a sensitivity of 92.86% and specifcity of 100% in distinguishing well-diferentiated embryonal rhabdomyosarcoma (ERMS) from fetal rhabdomyoma. Besides, the expression of EZH2 mRNA was higher in LMS and RMS than in benign tumors (p < 0.05). The expressions of SUZ12 and RbAp46 protein were higher in RMS than in rhabdomyoma (p < 0.05). Conclusively, the high expression of EZH2 is a promising marker in distinguishing well–diferentiated LMS from cellular leiomyoma, or well–diferentiated ERMS from fetal rhabdomyoma, and the upregulation of EZH2 protein expression may occur at transcriptional level. Overlap in morphologic features between malignant and benign myogenic tumors, such as well-diferentiated leiomyosarcoma (LMS) vs. cellular leiomyoma as well as well-diferentiated rhabdomyosarcoma (RMS) vs. fetal rhabdomyoma, ofen makes diferential diagnosis difcult and challenging. LMS mainly occurs in the pelvic retroperitoneum/abdomen of adults, with hypercellularity, nuclear atypia and active mitosis. However, well-diferentiated LMS, with no excessive mitotic activity and undue nuclear atypia, ofen shows histological features similar to cellular leiomyoma. Cellular leiomyoma ofen shows the morphology features of increased cellularity, large tumor size and active mitotic activity. RMS is one of the most common sarcomas with high recurrence rates in infants and children. Embryonal rhabdomyosarcoma (ERMS) is a subtype of RMS. Te well-diferentiated ERMS is sometimes indistinguishable from fetal rhabdomyoma for lacks of cytologic atypia and active mitosis. Fetal rhabdomyoma is rare and ofen considered to be a mimic of well-diferentiated ERMS. Immunohistochemical markers used for clinical diagnoses, such as MAS, vimentin, calponin, SMA and desmin, are not efective in diferentiating these malignant tumors from benign tumors. To address this issue, highly sen- sitive and specifc new markers are needed for diferential diagnosis. 1School of Basic Medicine, Shanghai University of Medicine and Health Sciences, Shanghai, 201318, People’s Republic of China. 2Department of Pathology, Renmin Hospital of Wuhan University, Wuhan, 430060, Hubei Provicne, People’s Republic of China. 3Pathology Center, Shanghai General Hospital/Faculty of Basic Medicine, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200025, People’s Republic of China. 4Second Department of Neurosurgery, The First Afliated Hospital of Kunming Medical University, Kunming, 650032, Yunnan Province, People’s Republic of China. 5School of Clinical Medicine, Shanghai University of Medicine and Health Sciences, Shanghai, 201318, People’s Republic of China. Ning Zhang and Zhi Zeng contributed equally to this work. Correspondence and requests for materials should be addressed to P.H. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:12331 | DOI:10.1038/s41598-018-30648-7 1 www.nature.com/scientificreports/ Enhancer of Zeste Homolog 2 (EZH2) is a key subunit of polycomb repressive complex 2 (PRC2) and represses its target genes by catalyzing histone methylation through the coordinate action of three other components of PRC2, including Suppressor of Zeste 12 (SUZ12), Embryonic Ectoderm Development (EED) and retinoblas- toma protein associated protein 46 (RbAp46). Previous studies have reported that high expression of EZH2 was found in various kinds of cancers, which contributed to tumor progression and poor prognosis1–9. In recent years, upregulation of EZH2 expression was also discovered in certain sarcomas, including Ewing sarcoma, RMS, syno- vial sarcoma, osteosarcoma and chondrosarcoma. Ewing sarcoma and RMS are common pediatric sarcomas with high malignance. Ramaglia10 found that EZH2 was expressed with a diferent degree in 60% of 17 patients with Ewing sarcoma or RMS and it was signifcantly higher in patients presenting lymph node and/or distant metasta- ses. Moreover, overexpression of EZH2 was positively relative to lower probability of survival. EZH2 expression can be induced by the fusion gene of EWS/FLI1 via binding to its promoter in Ewing sarcoma in vivo11. It was also demonstrated that EZH2 was aberrantly overexpressed in RMS primary tumors and cell lines, and downregula- tion of it in vitro can lead to muscle-like diferentiation of RMS cells12–14. Some studies exist on synovial sarcoma revealed that EZH2 expressed in 76% of patients15. EZH2 mRNA and protein were highly expressed in poorly diferentiated subtype. Even in the monophasic and biphasic subtypes, patients with high EZH2 score was charac- terized by high proliferation rate, large tumor size, distant metastasis and poor outcomes16. EZH2 overexpression was also detected in osteosarcoma17 and high grade chondrosarcomas18, which was signifcantly associated with aggressive behavior and poor prognosis. However, the expression of EZH2 in malignant myogenic tumors, such as LMS and RMS, remains unknown. Specifcally, the diference of its expression in malignant and benign tumors has not been elucidated yet. In this study, we detected the expression of EZH2 and three other components of PRC2 in 32 LMS, 51 RMS, 16 uterine leiomyoma, 15 rhabdomyoma as well as 31 normal tissues to evaluate the application value of EZH2 in dif- ferential diagnosis. In addition, the association between EZH2 expression and clinicopathological characteristics, and the correlation of EZH2 with ki-67 protein were assessed to identify the signifcance in these malignant tum- ors. We also investigated EZH2 mRNA expression by analyzing the Gene Expression Omnibus (GEO) Datasets. Results The EZH2 protein was highly expressed in LMS. In this study, immunohistochemical analysis was performed in 64 specimens, including 32 LMS, 16 uterine leiomyoma and 16 normal myometrial to quantify and localize the expression of EZH2 protein. Microscopy pictures showed nuclear localization of EHZ2 in LMS (Fig. 1). Totally, EZH2 protein expression was observed in 26 of 32 (81.25%) LMS, whereas none was found in uterine leiomyoma and normal myometrium (p < 0.05, Table 1). Of 32 LMS cases, 4 were scored 0 (negative staining), 2 were scored 1 (weak staining not exceeding 24% of tumor cells), 13 were scored 2 (weak staining between 25% to 49%), 16 were scored 2+ (moderate to strong staining exceeding 50%, Supplementary Table 1). Further subgroup analysis showed that EZH2 expression was found in 21 of 23 (91.30%) well-diferentiated and signifcancently higher than that in cellular uterine leiomyoma (p < 0.05) (Table 2). According to the tumor sites, LMS were divided into two groups: uterine LMS and extra-uterine LMS. No signifcant diference in EZH2 protein expres- sion level was found between the two groups (Table 3 and Supplementary Table 2). The EZH2 protein was highly expressed in RMS. In this study, the expression of EZH2 protein was measured in 81 cases, 51 from RMS and 15 from fetal rhabdomyoma, as well as in 15 specimens of tumor adjacent skeletal muscle (TASM). Microscopy pictures showed nuclear localization of EHZ2 in RMS (Fig. 2). EZH2 pro- tein expression was detected in 36 of 51 (70.58%) RMS, but not in rhabdomyoma and TASM (p < 0.05, Table 4). Of 51 RMS cases, 10 were scored 0 (negative staining), 5 were scored 1 (weak staining not exceeding 24%), 12 were scored 2 (weak staining between 25% to 49%), 24 were scored 2+ (moderate to strong staining exceeding 50%, Supplementary Table 3). Subgroup analysis indicated that EZH2 protein was found in 26 of 28 (92.86%) of well-diferentiated ERMS and signifcantly higher than that in fetal rhabdomyoma (p < 0.05, Table 5). High expression levels of EZH2 mRNA in LMS. Te data set GSE64763 (Fig. 3A) showed the relative expression levels of EZH2 mRNA in LMS (n = 25), uterine leiomyoma (n = 25) and normal myometrium (n = 28) were 1.56, 1.11 and 1, respectively. EZH2 mRNA expression in LMS were signifcantly higher than those in uter- ine leiomyoma and normal myometrium (p < 0.05). Te data set GSE764 (Fig. 3B) showed the relative expression levels of EZH2 mRNA in uterine LMS (n = 9), extra-uterine LMS (n = 4), uterine leiomyoma (n = 9) and normal myometrium (n = 4) were 2.54, 5.15, 0.64 and 1, respectively. Te expression of EZH2 mRNA in uterine and extra-uterine LMS were higher than those in uter- ine leiomyoma and normal myometrium (p < 0.05), respectively. And
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