Journal of Pathology and Translational Medicine

Original Article

Clinicopathological implications of immunohistochemical expression of TBX21, CXCR3, GATA3, CCR4, and TCF1 in nodal follicular helper T-cell lymphoma and peripheral T-cell lymphoma, not otherwise specified: Bogyeong Han, Sojung Lim, Jeemin Yim, Young Keun Song, Jiwon Koh, Sehui Kim, Cheol Lee, Young A Kim, Yoon Kyung Jeon; J Pathol Transl Med. 2024;58(2):59-71. Published online January 22, 2024; DOI: https://doi.org/10.4132/jptm.2024.01.04

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Abstract PDF Supplementary Material: Background
The classification of nodal peripheral T-cell lymphoma (PTCL) has evolved according to histology, cell-of-origin, and genetic alterations. However, the comprehensive expression pattern of follicular helper T-cell (Tfh) markers, T-cell factor-1 (TCF1), and Th1- and Th2-like molecules in nodal PTCL is unclear.
Methods
Eighty-two cases of nodal PTCL were classified into 53 angioimmunoblastic T-cell lymphomas (AITLs)/nodal T-follicular helper cell lymphoma (nTFHL)-AI, 18 PTCLs-Tfh/nTFHL–not otherwise specified (NOS), and 11 PTCLs-NOS according to the revised 4th/5th World Health Organization classifications. Immunohistochemistry for TCF1, TBX21, CXCR3, GATA3, and CCR4 was performed.
Results
TCF1 was highly expressed in up to 68% of patients with nTFHL but also in 44% of patients with PTCL-NOS (p > .05). CXCR3 expression was higher in AITLs than in non-AITLs (p = .035), whereas GATA3 expression was higher in non-AITL than in AITL (p = .007) and in PTCL-Tfh compared to AITL (p = .010). Of the cases, 70% of AITL, 44% of PTCLTfh/ nTFHL-NOS, and 36% of PTCL-NOS were subclassified as the TBX21 subtype; and 15% of AITL, 38% of PTCL-Tfh/nTFHL-NOS, and 36% of PTCL-NOS were subclassified as the GATA3 subtype. The others were an unclassified subtype. CCR4 expression was associated with poor progression-free survival (PFS) in patients with PTCL-Tfh (p < .001) and nTFHL (p = .023). The GATA3 subtype showed poor overall survival in PTCL-NOS compared to TBX21 (p = .046) and tended to be associated with poor PFS in patients with non-AITL (p = .054).
Conclusions
The TBX21 subtype was more prevalent than the GATA3 subtype in AITL. The GATA3 subtype was associated with poor prognosis in patients with non-AITL and PTCL-NOS.

Review

Molecular Testing of Lymphoproliferative Disorders: Current Status and Perspectives: Yoon Kyung Jeon, Sun Och Yoon, Jin Ho Paik, Young A Kim, Bong Kyung Shin, Hyun-Jung Kim, Hee Jeong Cha, Ji Eun Kim, Jooryung Huh, Young-Hyeh Ko; J Pathol Transl Med. 2017;51(3):224-241. Published online May 10, 2017; DOI: https://doi.org/10.4132/jptm.2017.04.09

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Molecular pathologic testing plays an important role for the diagnosis, prognostication and decision of treatment strategy in lymphoproliferative disease. Here, we briefly review the molecular tests currently used for lymphoproliferative disease and those which will be implicated in clinical practice in the near future. Specifically, this guideline addresses the clonality test for B- and T-cell proliferative lesions, molecular cytogenetic tests for malignant lymphoma, determination of cell-of-origin in diffuse large B-cell lymphoma, and molecular genetic alterations incorporated in the 2016 revision of the World Health Organization classification of lymphoid neoplasms. Finally, a new perspective on the next-generation sequencing for diagnostic, prognostic, and therapeutic purpose in malignant lymphoma will be summarized.

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Original Articles

Cancers with Higher Density of Tumor-Associated Macrophages Were Associated with Poor Survival Rates: Kyong Yeun Jung, Sun Wook Cho, Young A Kim, Daein Kim, Byung-Chul Oh, Do Joon Park, Young Joo Park; J Pathol Transl Med. 2015;49(4):318-324. Published online June 17, 2015; DOI: https://doi.org/10.4132/jptm.2015.06.01

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Abstract PDF

Background
Macrophages are a component of a tumor’s microenvironment and have various roles in tumor progression and metastasis. This study evaluated the relationships between tumor-associated macrophage (TAM) density and clinical outcomes in 14 different types of human cancers. Methods: We investigated TAM density in human tissue microarray sections from 14 different types of human cancers (n = 266) and normal thyroid, lung, and breast tissues (n = 22). The five-year survival rates of each cancer were obtained from the 2011 Korea Central Cancer Registry. Results: Among 13 human cancers, excluding thyroid cancer, pancreas, lung, and gallbladder cancers had the highest density of CD163-positive macrophages (7.0±3.5%, 6.9±7.4%, and 6.9 ± 5.5%, respectively). The five-year relative survival rates of these cancers (pancreas, 8.7%; lung, 20.7%; gallbladder, 27.5%) were lower than those of other cancers. The histological subtypes in thyroid cancer exhibited significantly different CD163-positive macrophages densities (papillary, 1.8 ± 1.6% vs anaplastic, 22.9 ± 17.1%; p < .001), but no significant difference between histological subtypes was detected in lung and breast cancers. Moreover, there was no significant difference in CD163-positive macrophages densities among the TNM stages in lung, breast, and thyroid cancers. Conclusions: Cancers with higher TAM densities (pancreas, lung, anaplastic thyroid, and gallbladder) were associated with poor survival rate.

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Detection of Survivin and COX-2 in Thyroid Carcinoma: Anaplastic Carcinoma Shows Overexpression of Nuclear Survivin and Low COX-2 Expression: Young A Kim, Meesoo Chang, Young Joo Park, Ji Eun Kim; Korean J Pathol. 2012;46(1):55-60. Published online February 23, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.1.55

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Abstract PDF

Background

Overexpression of survivin, a member of the inhibitors of apoptosis protein, has been reported in various carcinomas, and its interaction with cyclooxygenase 2 (COX-2) results in accelerated tumor progression. The purpose of this study is to investigate the immunohistochemical expression of survivin and COX-2 in benign and malignant thyroid tissues and to define its association with pathologic and clinical features.

Methods

We examined expression of survivin and COX-2 by immunohistochemistry in 334 benign and malignant thyroid tissues and evaluated their clinical significance.

Results

Expression of survivin showed an increase along the spectrum of thyroid carcinoma progression; rarely positive in adenomatous goiter, moderately positive in papillary carcinoma, and strongly positive in anaplastic carcinoma (AC). Papillary microcarcinoma revealed the highest COX-2 positivity and AC demonstrated the lowest positivity among thyroid cancers. Node negative carcinomas showed higher COX-2 expression than node positive tumors. Survivin expression did not correlate with COX-2.

Conclusions

Our findings suggest that survivin overexpression may be related to the pathogenesis of AC and can be a predictor of disease progression. COX-2 may be involved in the early phase of thyroid carcinoma.

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Survivin as a diagnostic and therapeutic marker for thyroid cancer
Mohammad-Reza Mahmoudian-Sani, Arash Alghasi, Ali Saeedi-Boroujeni, Akram Jalali, Mohammad Jamshidi, Ali Khodadadi
Pathology - Research and Practice.2019; 215(4): 619. CrossRef
TFAP2B overexpression contributes to tumor growth and progression of thyroid cancer through the COX-2 signaling pathway
Xiaoyan Fu, Huayong Zhang, Zhipeng Chen, Zhongyuan Yang, Dingbo Shi, Tianrun Liu, Weichao Chen, Fan Yao, Xuan Su, Wuguo Deng, Miao Chen, Ankui Yang
Cell Death & Disease.2019;[Epub] CrossRef
Expression of nm23-H1 and COX-2 in thyroid papillary carcinoma and microcarcinoma
Marija Milkovic Perisa, Bozena Sarcevic, Koraljka Gall Troselj, Kresimir Grsic, Sanda Sitic, Sven Seiwerth
Oncology Letters.2017; 13(5): 3547. CrossRef
The Diagnostic Usefulness of HMGA2, Survivin, CEACAM6, and SFN/14-3-3 δ in Follicular Thyroid Carcinoma
Min Hye Jang, Kyeong Cheon Jung, Hye Sook Min
Journal of Pathology and Translational Medicine.2015; 49(2): 112. CrossRef
Evaluation of survivin expression and its prognostic value in papillary thyroid carcinoma
Sonja Selemetjev, Tijana Isic Dencic, Ilona Marecko, Jelena Jankovic, Ivan Paunovic, Svetlana Savin, Dubravka Cvejic
Pathology - Research and Practice.2014; 210(1): 30. CrossRef

Expression of P-glycoprotein and Apoptosis in Diffuse Large B-cell Lymphoma.: Ji Eun Kim, Young A Kim, Mee Soo Chang, Yunkyeong Jeon, JinHo Paik, Seon Og Yoon; Korean J Pathol. 2009;43(4):317-320.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.4.317

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Abstract PDF: BACKGROUND
Diffuse large B-cell lymphoma (DLBCL) is the most common type of malignant lymphoma which responds well to conventional chemotherapy. However, quite a few patients have a recurrence with more aggressive forms after completion of therapy. Multidrug resistance proteins (MRP) are related to this process in several ways such as cell cycle alteration and modulation of apoptosis. METHODS: We investigated the expression of P-glycoprotein (Gp), one of the well-known MRP, as well as apoptosis associated proteins in DLBCL. Immunohistochemical staining for Gp, p53, Bcl-2, Ki-67, active caspase 3 and FADD was done in forty DLBCL cases. The association between MRP and apoptosis associated proteins to clinical findings was also tested. RESULTS: Twenty-nine patients out of 40 (73%) with DLBCL were positive for Gp, and 26 cases (65%) had a strong positive for Gp. Gp expression was stronger in high-grade lesions than in low-grade lesions and was associated to Bcl-2 expression. However, we could not find an adverse impact of Gp expression on patients' overall survival or relapse free survival rate. CONCLUSIONS: Our study revealed a high frequency of expression for Gp in DLBCL with a possible relationship between the expressions of Gp to apoptosis associated proteins.

Detection of SV40 Large T Antigen in Malignant Lymphomas.: Young A Kim, MeeSoo Chang, Jinho Paik, Sun Och Yoon, Yoon Kyung Jeon, Chul Woo Kim, Ji Eun Kim; Korean J Pathol. 2009;43(4):312-316.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.4.312

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Abstract PDF

BACKGROUND
The association of simian virus 40 (SV40) with certain types of human cancers, including malignant lymphomas, has been a topic of interest for some time. Although the virus is distributed worldwide, its incidences vary according to the specific types of tumors, and the epidemiological areas. The aim of this study was to investigate the frequency of SV40 in malignant lymphomas among Korean patients. METHODS: One hundred seventy three cases of malignant lymphomas were evaluated by immunohistochemical staining for SV40 large T antigen (TAg), using an extremely sensitive, tyramide based, catalyzed signal amplification method. RESULTS: From 158 non-Hodgkin's lymphomas, including 115 diffuse large B-cell lymphomas, and 15 Hodgkin's lymphomas, none of the cases were positive for SV40 TAg. CONCLUSIONS: SV40 does not appear to be related to the pathogenesis of malignant lymphomas among Koreans.

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No Detection of Simian Virus 40 in Malignant Mesothelioma in Korea
Minseob Eom, Jamshid Abdul-Ghafar, Sun-Mi Park, Joung Ho Han, Soon Won Hong, Kun Young Kwon, Eun Suk Ko, Lucia Kim, Wan Seop Kim, Seung Yeon Ha, Kyo Young Lee, Chang Hun Lee, Hye Kyoung Yoon, Yoo Duk Choi, Myoung Ja Chung, Soon-Hee Jung
Korean Journal of Pathology.2013; 47(2): 124. CrossRef

Clinicopathologic Study of Chromosomal Aberrations in Gastric Lymphomas of Korean Patients.: Wook Youn Kim, Jung Ho Kim, Hyoungsuk Ko, Young A Kim, Yoon Kyung Jeon, Chul Woo Kim; Korean J Pathol. 2009;43(1):5-12.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.1.5

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Abstract PDF

BACKGROUND
The incidence and clinical correlation of MALT1 translocation and numerical aberrations in Korean gastric MALT lymphoma patients have been rarely reported. We studied the incidence and clinicopathologic relationship of these chromosomal aberrations in Korean gastric lymphomas.
METHODS
Seventy-six gastric lymphomas, which consisted of 40 low grade MALT lymphoma, 4 high grade MALT lymphoma and 32 diffuse large B-cell lymphoma (DLBCL) cases, were analyzed for the detection of t(11;18) API2-MALT1, t(14;18) IgH-MALT1 and aneuploidies of chromosomes 3 or 18 using fluorescence in situ hybridization.
RESULTS
The t(11;18) was demonstrated in 3 low grade MALT lymphomas (7.5%) and one DLBCL, which was associated with advanced stage, deeper invasion, and disease progression or relapse. The t(14;18) was demonstrated in none of these cases. Trisomy 3 and 18 were detected in 8 (11%) and 11 of 76 cases (12.5%) respectively, and found only in translocation-negative cases. Two of 4 high grade MALT lymphomas showed trisomy 18. All patients survived with successful second treatment after progression or relapse.
CONCLUSIONS
The t(11;18) API2-MALT1 was not quite frequent in Korean low grade gastric MALT lymphomas and was associated with advanced clinical situations. Overall prognosis was good for long-term follow-up regardless of progression or relapse.

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Clinicopathologic Study of Chromosomal Aberrations in Ocular Adnexal Lymphomas of Korean Patients
Hokyung Choung, Young A Kim, Namju Kim, Min Joung Lee, Sang In Khwarg
Korean Journal of Ophthalmology.2015; 29(5): 285. CrossRef

Juvenile Hyaline Fibromatosis in an Adult.: Young A Kim, Seoung Wan Chae, Chong Jai Kim, Je G Chi; Korean J Pathol. 2000;34(3):239-242.

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Abstract PDF: Juvenile hyaline fibromatosis is a rare disorder probably inherited as an autosomal recessive trait. It is characterized by multiple slowly growing subcutaneous nodules, hypertrophy of gingiva, flexion contracture, and radiolucent bone destruction. The histological features of the tumor-like lesions are characterized by the deposition of amorphous hyaline material in which spindle shaped cells are embedded. We report a case of juvenile hyaline fibromatosis in a 26 year-old-woman. She had multiple subcutaneous nodules in scalp, ear, forearms, right knee, and back. Surgical excision of the tumors in the scalp and ear was done. The largest one measured 13 9 6 cm, and had homogeneous, grayish yellow cut surface with calcification. Light microscopic examination showed abundant eosinophilic hyaline material with extensive calcification and metaplastic bone formation. Spindle cells were rarely observed at the periphery of the tumor. Hyaline matrix was PAS positive, diastase resistant, and alcian blue negative. Scattered spindle cells were positive for vimentin but negative for S-100 protein and smooth muscle actin. There were many reports regarding early lesions of juvenile hyaline fibromatosis; however in this patient, tumor existed for more than 20 years and the histology was somewhat different from the early lesions reported in the literature.

Methylotion Analysis of p16/INK4A in Gastric Low-Grade Mucosa-Associated Lymphoid Tissue Lymphomas after Helicobacter pylori Eradication Therapy.: Young A Kim, Sung Shin Park, Bo Young Lee, You Sun Kim, In Sung Song, Chul Woo Kim; Korean J Pathol. 2002;36(1):13-20.

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Abstract PDF: BACKGROUND
Inactivation of p16 has been associated with promoter region hypermethylation in different types of malignancies, including non-Hodgkin's lymphomas (NHLs). This loss of p16 was found frequently in cases of mucosa-associated lymphoid tissue (MALT) lymphomas. Recent studies indicate that promoter hypermethylation is often an early event in tumor progression in the follow-up of NHLs.
METHODS
To investigate the usefulness of p16 methylation in the diagnosis and follow-up of gastric low-grade MALT lymphomas, we analyzed methylation status of p16 using methylation-specific polymerase chain reaction methods in the sequential biopsy specimens of 13 patients with gastric low-grade MALT lymphomas undergoing Helicobacter pylori eradication therapy.
RESULTS
Five of thriteen cases showed p16 hypermethylation upon diagnosis. In four of five methylation positive cases, abnormal methylation was detected in the specimen even after the treatment, although there were no histologic evidence of disease. This methylation disappeared in the later samples of two of the cases, and they have remained in complete remission. Immunohistochemically, the loss of p16 protein expression was detected in one of three methylation-positive cases, and in none of the methylation-negative cases.
CONCLUSIONS
These results suggest that p16 methylation is relatively fequent in low-grade gastric MALT lymphomas, and it may have clinical applications in the management and follow-up of low-grade gastric MALT lymphomas.

Diffuse Large B Cell Lymphoma Shows Distinct Methylation Profiles of the Tumor Suppressor Genes among the Non-Hodgkin's Lymphomas.: Sun Och Yoon, Young A Kim, Yoon Kyung Jeon, Ji Eun Kim, Gyeong Hoon Kang, Chul Woo Kim; Korean J Pathol. 2008;42(1):16-20.

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Abstract PDF: BACKGROUND
Aberrant methylation of CpG islands in promoter regions is one of the major mechanisms for silencing of tumor suppressor genes in various types of human cancers including non-Hodgkin's lymphomas (NHL). In this study, we investigated the aberrant promoter methylation status of known or suspected tumor suppressor genes in NHLs and compared the methylation profiles between B-cell and T/NK-cell NHLs.
METHODS
54 cases of B-cell NHLs and 16 cases of T/NK-cell NHLs were examined for the methylation status of eight genes using methylation specific PCR.
RESULTS
CpG islands methylation was variously found in eight genes as follows; DAPK (71%), MT1G (70%), p16 (53%), CDH1 (53%), THBS1 (56%), MGMT (27.1%), COX2 (13%), and RUNX3 (11.4%). In six cases (8 %), methylation was not observed in any of these genes. Overall methylation index of B-cell NHLs (0.48) was significantly higher than that of T/NK-cell NHLs (0.32). Of eight genes tested, THBS1 and CDH1 methylations were much more prominent in diffuse large B-cell lymphomas than in T/NK-cell NHLs or other B-cell NHLs.
CONCLUSION
This study suggests that aberrant CpG island methylation is a frequent event in NHLs, and diffuse large B-cell lymphomas show overlapping but distinct methylation profiles.

Expressions of Id-1 and Id-2 in Hyperplastic Thyroid Tissue and Thyroid Carcinoma.: Young A Kim, Young Joo Park, Do Joon Park, Seong Hoe Park, Ji Eun Kim; Korean J Pathol. 2006;40(1):60-65.

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Abstract PDF: BACKGROUND
Id proteins are a family of helix-loop-helix proteins and are regarded to be negative regulators of cell differentiation. In general, Id-1 and Id-2 expressions are upregulated during tumor development and progression in a variety of neoplasms, and these expressions may be associated with aggressive tumor behavior. However, little is known about the roles of Id-1 and Id-2 in thyroid neoplasms.
METHODS
The expressions of Id-1 and Id-2 were assessed immunohistochemically in 310 normal, hyperplastic, and neoplastic thyroid tissues using tissue microarrays.
RESULTS
Normal thyroid tissues rarely expressed Id-1 or Id-2. Moreover, whilst Id-1 expression was more elevated in malignant thyroid tissue than in hyperplastic thyroid tissue, Id-2 expression was more variable. No significant differences were observed between histologic subtypes of thyroid carcinomas with respect to Id-1 or Id-2 expression. Follicular adenomas showed higher expressions of Id-1 and Id-2 than thyroid carcinomas. No significant association was found between clinicopathological parameters and Id-1 expression, though Id-2 expression was significantly reduced in metastatic, stage IV tumors.
CONCLUSION
The expressions of Id-1 and Id-2 were elevated in hyperplastic and neoplastic thyroid tissues. However, neither appears suitable as a marker of malignancy or an aggressive phenotype, although Id-2 expression in advanced thyroid carcinomas may reflect a favorable prognosis.

Case Report

Histiocytic Sarcoma of the Spleen: A Case Report and Review of the Literature.: Jin Ho Paik, Yoon Kyung Jeon, Sung Shin Park, Hye Sook Min, Young A Kim, Ji Eun Kim, Chul Woo Kim; Korean J Pathol. 2005;39(5):356-359.

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Abstract PDF: True histiocytic sarcoma is an extremely rare tumor. Its clinicopathological features are not clearly understood. Here, we report the first Korean case of primary splenic histiocytic sarcoma. A 64-year-old female having refractory thrombocytopenia, anemia and splenic mass was admitted to the hospital, and received splenectomy. Grossly, spleen was enlarged up to 18 x 13 x 8 cm and occupied with multinodular masses. Microscopically, the masses were composed of atyical large cells with abudant cytoplasm and vesicular nuclei with prominent hemophagocytosis. The tumor cells were CD68 (+), S-100 protein (-), CD21 (-), CD1a (-). After splenectomy, thrombocytopenia and anemia were corrected. However two months later the symptoms recurred, and the patient died 15 months after splenectomy. This case shared the common clinicopathologic features with the several previously reported cases in other countries, represented by splenic mass formation and prominent hemophagocytosis associated with thrombocytopenia and anemia, often leading to poor outcome.

Original Article

Methylation Status of Epstein-Barr Virus Major Latent Promoter C in NK/T-cell Lymphoma and Peripheral T-cell Lymphoma.: Ji Eun Kim, Young A Kim, Sung Shin Park, Yoon Kyoun Jeon, Seung Sook Lee, Chul Woo Kim; Korean J Pathol. 2003;37(3):174-179.

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Abstract PDF: BACKGROUND
Both the Natural killer/T-cell lymphoma (NKTL) and the peripheral T-cell lymphoma (PTCL) are relatively prevalent in the Asian population, and they are strongly associated with the Epstein-Barr virus (EBV). These two diseases have several common pathologic features, but show somewhat different clinical presentations. The critical point in terms of differentiating of these disease groups might be the impact of EBV in pathogenesis, and the variable gene expression of EBV regulated by a major latent C promoter (Cp).
METHODS
We investigated 43 cases of NKTL and 30 cases of PTCL to evaluate EBV associated characteristics. EBV in situ hybridization was performed in all of the submitted cases. In the EBV positive cases, the methylation status of Cp which drives the expression of immunodominant viral nuclear protein, was examined by sensitive methylation specific PCR using paraffin embedded tissue.
RESULTS
EBV was found in 70% (30/43) of NKTL and 43% (13/30) of PTCL. Nasal and gastrointestinal lymphomas were predominantly NKTL. All of the successfully amplified cases of EBV positive NKTL and PTCL were of methylated Cp status.
CONCLUSIONS
The detection rate of EBV is high in NKTL, especially in the nasal area. The constantly methylated EBV Cp reflects the major role of Cp in regulating the EBV latency pattern and in helping EBV to avoid host immune system in both NKTL and PTCL.

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