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1
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Akita M, Yanagimoto H, Tsugawa D, Zen Y, Fukumoto T. Surgical interpretation of the WHO subclassification of intrahepatic cholangiocarcinoma: a narrative review. Surg Today 2025; 55:1-9. [PMID: 38563999 DOI: 10.1007/s00595-024-02825-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/02/2023] [Accepted: 02/14/2024] [Indexed: 04/04/2024]
Abstract
Intrahepatic cholangiocarcinoma (iCCA) has been subclassified by its gross morphology into the mass-forming (MF), periductal-infiltrating (PI), and intraductal growth (IG) types and their combinations. This classification correlates well with clinical features; for example, MF-iCCA has less lymph-node metastasis and a better prognosis than PI-iCCA. According to the recently accumulated evidence from histological investigations, the WHO classification endorsed a subclassification scheme in which iCCA cases are classified into small- and large-duct types. Small-duct iCCA is considered to originate from septal or smaller bile ducts and is characterized by less frequent lymph-node metastasis, a favorable prognosis, and an MF appearance. Large-duct iCCA arises around the second branch of the biliary tree and has more aggressive biology and distinct genetic abnormalities. According to the practice guidelines for iCCA from the Liver Cancer Study Group of Japan and the National Comprehensive Cancer Network, upfront surgery is recommended for iCCA without distant metastasis regardless of the morphological subtype, based on clinical experience. In consideration of the biological heterogeneity of iCCA, the treatment strategy for iCCA needs to be reconsidered based on the WHO subtypes.
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Affiliation(s)
- Masayuki Akita
- Department of Surgery, Division of Hepato-Biliary-Pancreatic Surgery, Kobe University Graduate School of Medicine, Kobe, 650-0017, Japan
| | - Hiroaki Yanagimoto
- Department of Surgery, Division of Hepato-Biliary-Pancreatic Surgery, Kobe University Graduate School of Medicine, Kobe, 650-0017, Japan.
| | - Daisuke Tsugawa
- Department of Surgery, Division of Hepato-Biliary-Pancreatic Surgery, Kobe University Graduate School of Medicine, Kobe, 650-0017, Japan
| | - Yoh Zen
- Institute of Liver Studies, King's College Hospital, London, UK
| | - Takumi Fukumoto
- Department of Surgery, Division of Hepato-Biliary-Pancreatic Surgery, Kobe University Graduate School of Medicine, Kobe, 650-0017, Japan
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2
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Lu Y, Quan J, Liu F, Huang B. Systematic pan-cancer analysis of the prognostic value of MECOM in human cancer. Discov Oncol 2024; 15:694. [PMID: 39576394 PMCID: PMC11584820 DOI: 10.1007/s12672-024-01599-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/07/2024] [Accepted: 11/18/2024] [Indexed: 11/25/2024] Open
Abstract
Recently, emerging evidence suggests an association between MECOM (MDS1 and EVI1 complex locus) and cancers. However, a comprehensive pan-cancer analysis to fully investigate this relationship is lacking. Herein, public platforms with large-scale genomics, including The Cancer Genome Atlas, Gene Expression Omnibus dataset, and the Human Protein Atlas were explored to investigate the prognostic and immunological roles of MECOM across certain cancer types. Our findings revealed differential expression of MECOM in various cancer types, indicating its potential to predict diverse clinical outcomes, such as overall survival time and disease-free survival time in patients with various malignancies. Additionally, we observed an association between the mutation burden in MECOM in various cancers and patient survival. Furthermore, the mechanism of MECOM-mediated oncogenesis was tentatively explored by immune infiltration analysis. This study provided a relatively comprehensive overview of the prognostic and immunological roles of MECOM in multiple cancers.
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Affiliation(s)
- Yingqiang Lu
- Department of Urology, Urology and Nephrology Center, Cancer Center, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, 158 Shangtang Road, Hangzhou, 310014, Zhejiang, China
| | - Jing Quan
- Department of Urology, Urology and Nephrology Center, Cancer Center, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, 158 Shangtang Road, Hangzhou, 310014, Zhejiang, China
| | - Feng Liu
- Department of Urology, Urology and Nephrology Center, Cancer Center, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, 158 Shangtang Road, Hangzhou, 310014, Zhejiang, China
| | - Banggao Huang
- Department of Urology, Urology and Nephrology Center, Cancer Center, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, 158 Shangtang Road, Hangzhou, 310014, Zhejiang, China.
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3
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Huang XH, Chen TX, Liu HL, Huang MW. A Review of Type 1 and Type 2 Intraductal Papillary Neoplasms of the Bile Duct. Curr Med Sci 2024; 44:485-493. [PMID: 38748369 DOI: 10.1007/s11596-024-2863-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/16/2023] [Accepted: 02/29/2024] [Indexed: 06/29/2024]
Abstract
Intraductal papillary neoplasm of the bile duct (IPNB) is a heterogeneous disease similar to intraductal papillary mucinous neoplasm of the pancreas. These lesions have been recognized as one of the three major precancerous lesions in the biliary tract since 2010. In 2018, Japanese and Korean pathologists reached a consensus, classifying IPNBs into type l and type 2 IPNBs. IPNBs are more prevalent in male patients in East Asia and are closely related to diseases such as cholelithiasis and schistosomiasis. From a molecular genetic perspective, IPNBs exhibit early genetic variations, and different molecular pathways may be involved in the tumorigenesis of type 1 and type 2 IPNBs. The histological subtypes of IPNBs include gastric, intestinal, pancreaticobiliary, or oncocytic subtypes, but type 1 IPNBs typically exhibit more regular and well-organized histological features than type 2 IPNBs and are more commonly found in the intrahepatic bile ducts with abundant mucin. Due to the rarity of these lesions and the absence of specific clinical and laboratory features, imaging is crucial for the preoperative diagnosis of IPNB, with local bile duct dilation and growth along the bile ducts being the main imaging features. Surgical resection remains the optimal treatment for IPNBs, but negative bile duct margins and the removal of lymph nodes in the hepatic hilum significantly improve the postoperative survival rates for patients with IPNBs.
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Affiliation(s)
- Xia-Hui Huang
- Department of General Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006, China
| | - Tian-Xiang Chen
- Department of General Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006, China
| | - Hong-Liang Liu
- Department of General Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006, China
| | - Ming-Wen Huang
- Department of General Surgery, The Second Affiliated Hospital of Nanchang University, Nanchang, 330006, China.
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Zhu SZ, Gao ZF, Liu XR, Wang XG, Chen F. Surgically treating a rare and asymptomatic intraductal papillary neoplasm of the bile duct: A case report. World J Clin Cases 2024; 12:367-373. [PMID: 38313650 PMCID: PMC10835693 DOI: 10.12998/wjcc.v12.i2.367] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/07/2023] [Revised: 11/28/2023] [Accepted: 12/26/2023] [Indexed: 01/11/2024] Open
Abstract
BACKGROUND Intraductal papillary neoplasms of the bile duct (IPNBs) are rare and characterized by papillary growth within the bile duct lumen. IPNB is similar to obstructive biliary pathology. In this report, we present an unexpected case of asymptomatic IPNB and consolidate our findings with the relevant literature to augment our understanding of this condition. Integrating relevant literature contributes to a more comprehensive understanding of the disease. CASE SUMMARY A 66-year-old Chinese male patient was admitted to our hospital for surgical intervention after gallstones were discovered during a routine physical examination. Preoperative imaging revealed a lesion on the left side of the liver, which raised the suspicion of IPNB. A laparoscopic left hemihepatectomy was performed, and subsequent histopathological examination confirmed the diagnosis of IPNB. At the 3-mo postoperative follow-up, the patient reported good recovery and no metastasis. IPNB can manifest both latently and asymptomatically. Radical surgical resection is the most effective treatment for IPNB. CONCLUSION Hepatic and biliary masses, should be considered to diagnose IPNB. Prompt surgery and vigilant follow-up are crucial in determining prognosis.
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Affiliation(s)
- Shen-Zhen Zhu
- Department of General Surgery, Jiaxing Second Hospital, Jiaxing 314000, Zhejiang Province, China
| | - Zhao-Feng Gao
- Department of Hepatobiliary Surgery, Jiaxing Second Hospital, Jiaxing 314000, Zhejiang Province, China
| | - Xiao-Rong Liu
- Department of Hepatobiliary Surgery, Jiaxing Second Hospital, Jiaxing 314000, Zhejiang Province, China
| | - Xiao-Guang Wang
- Department of Hepatobiliary Surgery, Jiaxing Second Hospital, Jiaxing 314000, Zhejiang Province, China
| | - Fei Chen
- Department of Hepatobiliary Surgery, Jiaxing Second Hospital, Jiaxing 314000, Zhejiang Province, China
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Benson KK, Sheel A, Rahman S, Esnakula A, Manne A. Understanding the Clinical Significance of MUC5AC in Biliary Tract Cancers. Cancers (Basel) 2023; 15:cancers15020433. [PMID: 36672382 PMCID: PMC9856870 DOI: 10.3390/cancers15020433] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/19/2022] [Revised: 12/30/2022] [Accepted: 01/04/2023] [Indexed: 01/11/2023] Open
Abstract
Biliary tract cancers (BTC) arise from biliary epithelium and include cholangiocarcinomas or CCA (including intrahepatic (ICC) and extrahepatic (ECC)) and gallbladder cancers (GBC). They often have poor outcomes owing to limited treatment options, advanced presentations, frequent recurrence, and poor response to available systemic therapy. Mucin 5AC (MUC5AC) is rarely expressed in normal biliary epithelium, but can be upregulated in tissues of benign biliary disease, premalignant conditions (e.g., biliary intraepithelial neoplasia), and BTCs. This mucin's numerous glycoforms can be divided into less-glycosylated immature and heavily-glycosylated mature forms. Reported MUC5AC tissue expression in BTC varies widely, with some associations based on cancer location (e.g., perihilar vs. peripheral ICC). Study methods were variable regarding cancer subtypes, expression positivity thresholds, and MUC5AC glycoforms. MUC5AC can be detected in serum of BTC patients at high concentrations. The hesitancy in developing MUC5AC into a clinically useful biomarker in BTC management is due to variable evidence on the diagnostic and prognostic value. Concrete conclusions on tissue MUC5AC are difficult, but serum detection might be relevant for diagnosis and is associated with poor prognosis. Future studies are needed to further the understanding of the potential clinical value of MUC5AC in BTC, especially regarding predictive and therapeutic value.
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Affiliation(s)
- Katherine K. Benson
- Department of Internal Medicine, The Ohio State University College of Medicine, Columbus, OH 43210, USA
| | - Ankur Sheel
- Department of Internal Medicine, The Ohio State University College of Medicine, Columbus, OH 43210, USA
| | - Shafia Rahman
- Department of Internal Medicine, Division of Medical Oncology at the Arthur G. James Cancer Hospital and Richard J. Solove Research Institute, The Ohio State University Comprehensive Cancer Center, Columbus, OH 43210, USA
| | - Ashwini Esnakula
- Department of Pathology, The Ohio State University Wexner Medical Center, Columbus, OH 43210, USA
| | - Ashish Manne
- Department of Internal Medicine, Division of Medical Oncology at the Arthur G. James Cancer Hospital and Richard J. Solove Research Institute, The Ohio State University Comprehensive Cancer Center, Columbus, OH 43210, USA
- Correspondence: ; Tel.: +1-614-366-2982
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Gao X, Zhang W, Jia Y, Xu H, Zhu Y, Pei X. Identification of a prognosis-related ceRNA network in cholangiocarcinoma and potentially therapeutic molecules using a bioinformatic approach and molecular docking. Sci Rep 2022; 12:16247. [PMID: 36171401 PMCID: PMC9519560 DOI: 10.1038/s41598-022-20362-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/28/2022] [Accepted: 09/12/2022] [Indexed: 11/20/2022] Open
Abstract
Cholangiocarcinoma (CCA) is a highly malignant disease with a poor prognosis, and mechanisms of initiation and development are not well characterized. It is long noncoding RNAs (lncRNAs) acting as miRNA decoys to regulate cancer-related RNAs in competing endogenous RNA (ceRNA) networks that suggest a possible molecular mechanism in CCA. The current study aims to find potential prognosis biomarkers and small molecule therapeutic targets based on the construction of a CCA prognosis-related ceRNA network. A transcriptome dataset for CCA was downloaded from the TCGA database. Differentially expressed lncRNAs (DElncRNAs), DEmiRNAs and DEmRNAs were identified based on the differential expression and a DEceRNA network was constructed using predicted miRNA-lncRNA and miRNA-mRNA interactions. Heat maps, PCA analysis, and Pathway enrichment analysis and GO enrichment analysis were conducted. The prognostic risk model and molecular docking were constructed based on identified key ceRNA networks. A DElncRNA-miRNA-mRNAs network consisting of 434 lncRNA-miRNA pairs and 284 miRNA-mRNA pairs with 200 lncRNAs, 21 miRNAs, and 245 mRNAs was constructed. There were three lncRNAs (AC090772.1, LINC00519, and THAP7-AS1) and their downstream mRNAs (MECOM, MBNL3, RCN2) screened out as prognostic factors in CAA. Three key networks (LINC00519/ hsa-mir-22/ MECOM, THAP7-AS1/hsa-mir-155/MBNL3, and THAP7-AS1/hsa-mir-155/RCN2) were identified based on binding sites prediction and survival analysis. A prognostic risk model was established with a good predictive ability (AUC = 0.66–0.83). Four anticancer small molecules, MECOM and 17-alpha-estradiol (−7.1 kcal/mol), RCN2 and emodin (−8.3 kcal/mol), RCN2 and alpha-tocopherol (−5.6 kcal/mol), and MBNL3 and 17-beta-estradiol (−7.1 kcal/mol) were identified. Based on the DEceRNA network and Kaplan–Meier survival analysis, we identified three important ceRNA networks associated with the poor prognosis of CCA. Four anti-cancer small molecules were screened out by computer-assisted drug screening as potential small molecules for the treatment of CCA. This study provides theoretical support for the development of ceRNA network-based drugs to improve the prognosis of CCA.
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Affiliation(s)
- Xiaoling Gao
- The Medical Laboratory Center, Hainan General Hospital, Haikou, 570311, China.
| | - Wenhao Zhang
- The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730000, China
| | - Yanjuan Jia
- NHC Key Laboratory of Diagnosis and Therapy of Gastrointestinal Tumor, Gansu Provincial Hospital, Lanzhou, 730000, China.,The Institute of Clinical Research and Translational Medicine, Gansu Provincial Hospital, Lanzhou, 730000, China.,Gansu University of Chinese Medicine, Lanzhou, 730000, China
| | - Hui Xu
- NHC Key Laboratory of Diagnosis and Therapy of Gastrointestinal Tumor, Gansu Provincial Hospital, Lanzhou, 730000, China.,The Institute of Clinical Research and Translational Medicine, Gansu Provincial Hospital, Lanzhou, 730000, China
| | - Yuchen Zhu
- The Second Clinical Medical College, Lanzhou University, Lanzhou, 730000, China
| | - Xiong Pei
- The Second Clinical Medical College, Lanzhou University, Lanzhou, 730000, China
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7
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EVI1 Promotes the Proliferation and Invasive Properties of Human Head and Neck Squamous Cell Carcinoma Cells. Int J Mol Sci 2022; 23:ijms23031050. [PMID: 35162973 PMCID: PMC8835242 DOI: 10.3390/ijms23031050] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/17/2021] [Revised: 01/13/2022] [Accepted: 01/17/2022] [Indexed: 01/27/2023] Open
Abstract
Head and neck squamous cell carcinoma (HNSCC) is a frequent malignancy with a poor prognosis. So far, the EGFR inhibitor cetuximab is the only approved targeted therapy. A deeper understanding of the molecular and genetic basis of HNSCC is needed to identify additional targets for rationally designed, personalized therapeutics. The transcription factor EVI1, the major product of the MECOM locus, is an oncoprotein with roles in both hematological and solid tumors. In HNSCC, high EVI1 expression was associated with an increased propensity to form lymph node metastases, but its effects in this tumor entity have not yet been determined experimentally. We therefore overexpressed or knocked down EVI1 in several HNSCC cell lines and determined the impact of these manipulations on parameters relevant to tumor growth and invasiveness, and on gene expression patterns. Our results revealed that EVI1 promoted the proliferation and migration of HNSCC cells. Furthermore, it augmented tumor spheroid formation and the ability of tumor spheroids to displace an endothelial cell layer. Finally, EVI1 altered the expression of numerous genes in HNSCC cells, which were enriched for Gene Ontology terms related to its cellular functions. In summary, EVI1 represents a novel oncogene in HNSCC that contributes to cellular proliferation and invasiveness.
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8
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Zhang XM, Liu ZL, Qiu B, Xu YF, Pan C, Zhang ZL. Downregulation of EVI1 Expression Inhibits Cell Proliferation and Induces Apoptosis in Hilar Cholangiocarcinoma via the PTEN/AKT Signalling Pathway. J Cancer 2020; 11:1412-1423. [PMID: 32047548 PMCID: PMC6995371 DOI: 10.7150/jca.31903] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2018] [Accepted: 11/27/2019] [Indexed: 12/19/2022] Open
Abstract
Aims: Hilar cholangiocarcinoma (HCCA) is a tumour with high malignancy, low surgical resection potential, and a poor prognosis. Ecotropic Viral Integration site 1 (EVI1) is a transcriptional regulator that has been proven to be associated with tumourigenesis and progression in many human solid tumours. However, the expression of EVI1 and its role in HCCA progression remain unclear. The aim of this study was to clarify the association between EVI1 expression and clinical outcomes in patients with HCCA. Methods: The expression of EVI1 in HCCA tissue samples and cell lines was examined by quantitative real-time PCR (qRT-PCR), Western blotting, and immunohistochemistry (IHC). Kaplan-Meier analysis was used for survival analysis. A log-rank test was performed for univariate analysis of survival, and a Cox regression model was utilized for multivariate analysis of survival. Cell proliferation was measured by cell counting kit-8 (CCK-8), colony formation, and 5-ethynyl-2'-deoxyuridine (EdU) assays. The cell cycle was evaluated by flow cytometry. Cell apoptosis was detected by flow cytometry and a terminal deoxynucleotidyl transferase (TdT)-mediated dUTP nick-end labelling (TUNEL) assay. In vivo tumour growth was observed for xenografts in nude mice. Results: EVI1 expression was upregulated in HCCA tissue samples and correlated with a poor prognosis. In clinical specimens, the expression of EVI1 correlated with tumour histological grade and tumour size. Knocking down EVI1 expression reduced HCCA cell proliferation, blocked cell cycle progression, and promoted apoptosis in vitro and in vivo. Furthermore, we found that EVI1 could regulate the AKT signalling pathway by regulating PTEN levels in HCCA. Conclusion: Our data revealed that EVI1 played important roles in HCCA tumourigenesis and development. Our findings suggest that EVI1 may be a potentially useful therapeutic target in HCCA.
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Affiliation(s)
- Xiao-Ming Zhang
- Department of general surgery, Qilu Hospital of Shandong University, No. 107, Wenhua Xi Road, Jinan, 250012, China.,Department of general surgery, Linyi People's Hospital, Linyi, 276000, China
| | - Zeng-Li Liu
- Department of general surgery, Qilu Hospital of Shandong University, No. 107, Wenhua Xi Road, Jinan, 250012, China
| | - Bo Qiu
- Department of general surgery, Qilu Hospital of Shandong University (Qingdao), 266035, China
| | - Yun-Fei Xu
- Department of general surgery, Qilu Hospital of Shandong University, No. 107, Wenhua Xi Road, Jinan, 250012, China
| | - Chang Pan
- Department of emergency, Qilu Hospital of Shandong University, No. 107, Wenhua Xi Road, Jinan, 250012, China
| | - Zong-Li Zhang
- Department of general surgery, Qilu Hospital of Shandong University, No. 107, Wenhua Xi Road, Jinan, 250012, China
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Koroknai V, Szász I, Hernandez-Vargas H, Fernandez-Jimenez N, Cuenin C, Herceg Z, Vízkeleti L, Ádány R, Ecsedi S, Balázs M. DNA hypermethylation is associated with invasive phenotype of malignant melanoma. Exp Dermatol 2020; 29:39-50. [PMID: 31602702 DOI: 10.1111/exd.14047] [Citation(s) in RCA: 31] [Impact Index Per Article: 6.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/06/2019] [Revised: 08/29/2019] [Accepted: 10/06/2019] [Indexed: 01/01/2023]
Abstract
Tumor cell invasion is one of the key processes during cancer progression, leading to life-threatening metastatic lesions in melanoma. As methylation of cancer-related genes plays a fundamental role during tumorigenesis and may lead to cellular plasticity which promotes invasion, our aim was to identify novel epigenetic markers on selected invasive melanoma cells. Using Illumina BeadChip assays and Affymetrix Human Gene 1.0 microarrays, we explored the DNA methylation landscape of selected invasive melanoma cells and examined the impact of DNA methylation on gene expression patterns. Our data revealed predominantly hypermethylated genes in the invasive cells affecting the neural crest differentiation pathway and regulation of the actin cytoskeleton. Integrative analysis of the methylation and gene expression profiles resulted in a cohort of hypermethylated genes (IL12RB2, LYPD6B, CHL1, SLC9A3, BAALC, FAM213A, SORCS1, GPR158, FBN1 and ADORA2B) with decreased expression. On the other hand, hypermethylation in the gene body of the EGFR and RBP4 genes was positively correlated with overexpression of the genes. We identified several methylation changes that can have role during melanoma progression, including hypermethylation of the promoter regions of the ARHGAP22 and NAV2 genes that are commonly altered in locally invasive primary melanomas as well as during metastasis. Interestingly, the down-regulation of the methylcytosine dioxygenase TET2 gene, which regulates DNA methylation, was associated with hypermethylated promoter region of the gene. This can probably lead to the observed global hypermethylation pattern of invasive cells and might be one of the key changes during the development of malignant melanoma cells.
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Affiliation(s)
- Viktória Koroknai
- Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- MTA-DE Public Health Research Group, Public Health Research Institute, University of Debrecen, Debrecen, Hungary
| | - István Szász
- Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- MTA-DE Public Health Research Group, Public Health Research Institute, University of Debrecen, Debrecen, Hungary
| | | | | | - Cyrille Cuenin
- Epigenetics Group, International Agency for Research on Cancer (IARC), Lyon, France
| | - Zdenko Herceg
- Epigenetics Group, International Agency for Research on Cancer (IARC), Lyon, France
| | - Laura Vízkeleti
- Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- MTA-DE Public Health Research Group, Public Health Research Institute, University of Debrecen, Debrecen, Hungary
| | - Róza Ádány
- Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- MTA-DE Public Health Research Group, Public Health Research Institute, University of Debrecen, Debrecen, Hungary
| | - Szilvia Ecsedi
- Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- MTA-DE Public Health Research Group, Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- Epigenetics Group, International Agency for Research on Cancer (IARC), Lyon, France
| | - Margit Balázs
- Public Health Research Institute, University of Debrecen, Debrecen, Hungary
- MTA-DE Public Health Research Group, Public Health Research Institute, University of Debrecen, Debrecen, Hungary
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