Journal of Pathology and Translational Medicine

Volume 50(4); July 2016

Original Articles

Aquaporin 1 Is an Independent Marker of Poor Prognosis in Lung Adenocarcinoma: Sumi Yun, Ping-Li Sun, Yan Jin, Hyojin Kim, Eunhyang Park, Soo Young Park, Kyuho Lee, Kyoungyul Lee, Jin-Haeng Chung; J Pathol Transl Med. 2016;50(4):251-257. Published online June 7, 2016; DOI: https://doi.org/10.4132/jptm.2016.03.30

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Background
Aquaporin 1 (AQP1) overexpression has been shown to be associated with uncontrolled cell replication, invasion, migration, and tumor metastasis. We aimed to evaluate AQP1 expression in lung adenocarcinomas and to examine its association with clinicopathological features and prognostic significance. We also investigated the association between AQP1 overexpression and epithelial-mesenchymal transition (EMT) markers.
Methods
We examined AQP1 expression in 505 cases of surgically resected lung adenocarcinomas acquired at the Seoul National University Bundang Hospital from 2003 to 2012. Expression of AQP1 and EMT-related markers, including Ecadherin and vimentin, were analyzed by immunohistochemistry and tissue microarray.
Results
AQP1 overexpression was associated with several aggressive pathological parameters, including venous invasion, lymphatic invasion, and tumor recurrence. AQP1 overexpression tended to be associated with higher histological grade, advanced pathological stage, and anaplastic lymphoma kinase (ALK) translocation; however, these differences were not statistically significant. In addition, AQP1 overexpression positively correlated with loss of E-cadherin expression and acquired expression of vimentin. Lung adenocarcinoma patients with AQP1 overexpression showed shorter progression- free survival (PFS, 46.1 months vs. 56.2 months) compared to patients without AQP1 overexpression. Multivariate analysis confirmed that AQP1 overexpression was significantly associated with shorter PFS (hazard ratio, 1.429; 95% confidence interval, 1.033 to 1.977; p=.031).
Conclusions
AQP1 overexpression was thereby concluded to be an independent factor of poor prognosis associated with shorter PFS in lung adenocarcinoma. These results suggested that AQP1 overexpression might be considered as a prognostic biomarker of lung adenocarcinoma.

Citations

Citations to this article as recorded by

The Expanding Role of Aquaporin-1, Aquaporin-3 and Aquaporin-5 as Transceptors: Involvement in Cancer Development and Potential Druggability
Catarina Pimpão, Inês V. da Silva, Graça Soveral
International Journal of Molecular Sciences.2025; 26(3): 1330. CrossRef
The comprehensive potential of AQP1 as a tumor biomarker: evidence from kidney neoplasm cohorts, cell experiments and pan-cancer analysis
Yifan Liu, Donghao Lyu, Yuntao Yao, Jinming Cui, Jiangui Liu, Zikuan Bai, Zihui Zhao, Yuanan Li, Bingnan Lu, Keqin Dong, Xiuwu Pan
Human Genomics.2025;[Epub] CrossRef
Clinical application of cold atmospheric-pressure plasma: mechanisms and irradiation conditions
Eun Ji Jeong, Hyun Min Park, Dong Jae Lee, Jun Lee, Jun Yeong Cho, Kyung Deok Seo, Seokjun Je, Min Hyung Jung, Woo Yeon Hwang, Kyung Sook Kim
Journal of Physics D: Applied Physics.2024; 57(37): 373001. CrossRef
Aquaporins in Cancer Biology
Chul So Moon, David Moon, Sung Koo Kang
Frontiers in Oncology.2022;[Epub] CrossRef
A Comprehensive Prognostic Analysis of Tumor-Related Blood Group Antigens in Pan-Cancers Suggests That SEMA7A as a Novel Biomarker in Kidney Renal Clear Cell Carcinoma
Yange Wang, Chenyang Li, Xinlei Qi, Yafei Yao, Lu Zhang, Guosen Zhang, Longxiang Xie, Qiang Wang, Wan Zhu, Xiangqian Guo
International Journal of Molecular Sciences.2022; 23(15): 8799. CrossRef
Differential modulation of lung aquaporins among other pathophysiological markers in acute (Cl2 gas) and chronic (carbon nanoparticles, cigarette smoke) respiratory toxicity mouse models
Sukanta S. Bhattacharya, Brijesh Yadav, Ekta Yadav, Ariel Hus, Niket Yadav, Perminder Kaur, Lauren Rosen, Roman Jandarov, Jagjit S. Yadav
Frontiers in Physiology.2022;[Epub] CrossRef
Aquaporin water channels as regulators of cell-cell adhesion proteins
Sarannya Edamana, Frédéric H. Login, Soichiro Yamada, Tae-Hwan Kwon, Lene N. Nejsum
American Journal of Physiology-Cell Physiology.2021; 320(5): C771. CrossRef
Targeting Aquaporins in Novel Therapies for Male and Female Breast and Reproductive Cancers
Sidra Khan, Carmela Ricciardelli, Andrea J. Yool
Cells.2021; 10(2): 215. CrossRef
Targeting ion channels for the treatment of lung cancer
Liqin Zhang, Shuya Bing, Mo Dong, Xiaoqiu Lu, Yuancheng Xiong
Biochimica et Biophysica Acta (BBA) - Reviews on Cancer.2021; 1876(2): 188629. CrossRef
Comprehensive Analysis of Aquaporin Superfamily in Lung Adenocarcinoma
Guofu Lin, Luyang Chen, Lanlan Lin, Hai Lin, Zhifeng Guo, Yingxuan Xu, Chanchan Hu, Jinglan Fu, Qinhui Lin, Wenhan Chen, Yiming Zeng, Yuan Xu
Frontiers in Molecular Biosciences.2021;[Epub] CrossRef
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Aquaporin 1, 3, and 5 Patterns in Salivary Gland Mucoepidermoid Carcinoma: Expression in Surgical Specimens and an In Vitro Pilot Study
Mérin Barbara Stamboni, Ágatha Nagli de Mello Gomes, Milena Monteiro de Souza, Katia Klug Oliveira, Claudia Fabiana Joca Arruda, Fernanda de Paula, Barbara Beltrame Bettim, Márcia Martins Marques, Luiz Paulo Kowalski, Clóvis Antônio Lopes Pinto, Victor El
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Ekta Yadav, Niket Yadav, Ariel Hus, Jagjit S. Yadav
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Immunohistochemical Expression of Aquaporin-1 in Fluoro-Edenite-Induced Malignant Mesothelioma: A Preliminary Report
Giuseppe Angelico, Rosario Caltabiano, Carla Loreto, Antonio Ieni, Giovanni Tuccari, Caterina Ledda, Venerando Rapisarda
International Journal of Molecular Sciences.2018; 19(3): 685. CrossRef
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Michael L. De Ieso, Andrea J. Yool
Frontiers in Chemistry.2018;[Epub] CrossRef
Aquaporin 1 suppresses apoptosis and affects prognosis in esophageal squamous cell carcinoma
Yuzo Yamazato, Atsushi Shiozaki, Daisuke Ichikawa, Toshiyuki Kosuga, Katsutoshi Shoda, Tomohiro Arita, Hirotaka Konishi, Shuhei Komatsu, Takeshi Kubota, Hitoshi Fujiwara, Kazuma Okamoto, Mitsuo Kishimoto, Eiichi Konishi, Yoshinori Marunaka, Eigo Otsuji
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Hideko Imaizumi, Keiichiro Ishibashi, Seiichi Takenoshita, Hideyuki Ishida
Oncology Letters.2018;[Epub] CrossRef
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Xunwei Huang, Li Huang, Minhua Shao
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Guido Bellezza, Jacopo Vannucci, Fortunato Bianconi, Giulio Metro, Rachele Del Sordo, Marco Andolfi, Ivana Ferri, Paola Siccu, Vienna Ludovini, Francesco Puma, Angelo Sidoni, Lucio Cagini
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Transformation to Small Cell Lung Cancer of Pulmonary Adenocarcinoma: Clinicopathologic Analysis of Six Cases: Soomin Ahn, Soo Hyun Hwang, Joungho Han, Yoon-La Choi, Se-Hoon Lee, Jin Seok Ahn, Keunchil Park, Myung-Ju Ahn, Woong-Yang Park; J Pathol Transl Med. 2016;50(4):258-263. Published online May 10, 2016; DOI: https://doi.org/10.4132/jptm.2016.04.19

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Abstract PDF

Background
Epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors (TKIs) are considered the first line treatment for a subset of EGFR-mutated non-small cell lung cancer (NSCLC) patients. Although transformation to small cell lung cancer (SCLC) is one of the known mechanisms of resistance to EGFR TKIs, it is not certain whether transformation to SCLC is exclusively found as a mechanism of TKI resistance in EGFR-mutant tumors.
Methods
We identified six patients with primary lung adenocarcinoma that showed transformation to SCLC on second biopsy (n = 401) during a 6-year period. Clinicopathologic information was analyzed and EGFR mutation results were compared between initial and second biopsy samples.
Results
Six patients showed transformation from adenocarcinoma to SCLC, of which four were pure SCLCs and two were combined adenocarcinoma and SCLCs. Clinically, four cases were EGFR-mutant tumors from non-smoking females who underwent TKI treatment, and the EGFR mutation was retained in the transformed SCLC tumors. The remaining two adenocarcinomas were EGFR wild-type, and one of these patients received EGFR TKI treatment.
Conclusions
NSCLC can acquire a neuroendocrine phenotype with or without EGFR TKI treatment.

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Significance of Parafibromin Expression in Laryngeal Squamous Cell Carcinomas: Inju Cho, Mija Lee, Sharon Lim, Ran Hong; J Pathol Transl Med. 2016;50(4):264-269. Published online June 23, 2016; DOI: https://doi.org/10.4132/jptm.2016.04.24

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Abstract PDF

Background
Parafibromin is a product of the tumor suppressor gene that has been studied as a potential indicator of tumor aggressiveness in the parathyroid, breast, colorectum, and stomach. However, the clinical significance and potential function of parafibromin expression in head and neck squamous cell carcinomas remain largely unknown. The aim of this study was to evaluate the expression of parafibromin in laryngeal squamous cell carcinoma (LSCC) and to verify its potential as a biomarker of tumor behavior.
Methods
Parafibromin expression was evaluated in 30 cases of LSCC using immunohistochemistry. The correlations between parafibromin expression and clinicopathologic parameters were investigated.
Results
Parafibromin expression was positive in 15 cases (50%) and negative in 15 cases (50%). Tumor size and T stage showed a statistically significant inverse relationship with parafibromin expression (p=.028 and p<.001, respectively). Parafibromin expression was not associated with age, sex, lymph node metastasis, tumor differentiation, or tumor location. There was no statistically significant relationship between parafibromin expression and progression-free survival in the patients (p>.05).
Conclusions
Our results indicate that the downregulation or loss of parafibromin expression can be employed as a novel marker of tumor progression or aggressiveness in LSCC.

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CDC73 c.1155-3A>G is a pathogenic variant that causes aberrant splicing, disrupted parafibromin expression, and hyperparathyroidism-jaw tumor syndrome
Leor Needleman, Nicolette Chun, Sathvika Sitaraman, Marilyn Tan, Deborah E Sellmeyer, Electron Kebebew, Justin P Annes
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Advances in the application of label‐free quantitative proteomics techniques in malignancy research
Xiao Meng, Dong Liu, Yan Guan
Biomedical Chromatography.2023;[Epub] CrossRef
The roles of the tumor suppressor parafibromin in cancer
Hua-chuan Zheng, Hang Xue, Cong-yu Zhang
Frontiers in Cell and Developmental Biology.2022;[Epub] CrossRef
The clinicopathological and prognostic significances of CDC73 expression in cancers: a bioinformatics analysis
Hua-Chuan Zheng, Bao-Cheng Gong, Shuang Zhao
Oncotarget.2017; 8(56): 95270. CrossRef

Stromal Expression of MicroRNA-21 in Advanced Colorectal Cancer Patients with Distant Metastases: Kyu Sang Lee, Soo Kyung Nam, Jiwon Koh, Duck-Woo Kim, Sung-Bum Kang, Gheeyoung Choe, Woo Ho Kim, Hye Seung Lee; J Pathol Transl Med. 2016;50(4):270-277. Published online May 31, 2016; DOI: https://doi.org/10.4132/jptm.2016.03.19

9,384 View
98 Download
21 Web of Science
17 Crossref

Abstract PDF

Background
The aim of this study was to determine the regional heterogeneity and clinicopathological significance of microRNA-21 (miR-21) in advanced colorectal cancer (CRC) patients with distant metastasis.
Methods
miR-21 expression was investigated by using locked nucleic acid– fluorescence in situ hybridization in the center and periphery of the primary cancer and in distant metastasis from 170 patients with advanced CRC. In addition, α-smooth muscle actin and desmin were evaluated to identify cancer-associated fibroblasts (CAFs) by using immunohistochemistry.
Results
The miR-21 signal was observed in the cancer stroma. The expression of miR-21 (a score of 1–4) in the center and periphery of the primary cancer and in distant metastasis was observed in specimens from 133 (78.2%), 105 (61.8%), and 91 (53.5%) patients, respectively. miR-21 expression was heterogeneous in advanced CRC. Discordance between miR-21 expression in the center of the primary cancer and either the periphery of the primary cancer or distant metastasis was 31.7% or 44.7%, respectively. miR-21 stromal expression in the periphery of the primary cancer was significantly associated with a better prognosis (p=.004). miR-21 expression was significantly associated with CAFs in the center of the primary cancer (p=.001) and distant metastases (p=.041).
Conclusions
miR-21 expression is observed in cancer stroma related to the CAF quantity and frequently presents regional heterogeneity in CRC. Our findings indicate that the role of miR-21 in predicting prognosis may be controversial but provide a new perspective of miR-21 level measurement in cancer specimens.

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Exosomal miRNAs and miRNA dysregulation in cancer-associated fibroblasts
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Jiwon Koh, Chan-Young Ock, Jin Won Kim, Soo Kyung Nam, Yoonjin Kwak, Sumi Yun, Sang-Hoon Ahn, Do Joong Park, Hyung-Ho Kim, Woo Ho Kim, Hye Seung Lee
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Detection of Tumor Multifocality Is Important for Prediction of Tumor Recurrence in Papillary Thyroid Microcarcinoma: A Retrospective Study and Meta-Analysis: Jung-Soo Pyo, Jin Hee Sohn, Guhyun Kang; J Pathol Transl Med. 2016;50(4):278-286. Published online June 6, 2016; DOI: https://doi.org/10.4132/jptm.2016.03.29

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Abstract PDF

Background
The clinicopathological characteristics and conclusive treatment modality for multifocal papillary thyroid microcarcinoma (mPTMC) have not been fully established.
Methods
A retrospective study, systematic review, and meta-analysis were conducted to elucidate the clinicopathological significance of mPTMC. We investigated the multiplicity of 383 classical papillary thyroid microcarcinomas (PTMCs) and the clinicopathological significance of incidental mPTMCs. Correlation between tumor recurrence and multifocality in PTMCs was evaluated through a systematic review and meta-analysis.
Results
Tumor multifocality was identified in 103 of 383 PTMCs (26.9%). On linear regression analysis, primary tumor diameter was significantly correlated with tumor number (R²=0.014, p=.021) and supplemental tumor diameter (R²=0.117, p=.023). Of 103 mPTMCs, 61 (59.2%) were non-incidental, with tumor detected on preoperative ultrasonography, and 42 (40.8%) were diagnosed (incidental mPTMCs) on pathological examination. Lymph node metastasis and higher tumor stage were significantly correlated with tumor multifocality. However, there was no difference in nodal metastasis or tumor stage between incidental and non-incidental mPTMCs. On meta-analysis, tumor multifocality was significantly correlated with tumor recurrence in PTMCs (odds ratio, 2.002; 95% confidence interval, 1.475 to 2.719, p<.001).
Conclusions
Our results show that tumor multifocality in PTMC, regardless of manner of detection, is significantly correlated with aggressive tumor behavior.

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CrossRef Listing of Deleted DOIs.2000;[Epub] CrossRef

Morphometric Analysis of Thyroid Follicular Cells with Atypia of Undetermined Significance: Youngjin Kang, Yoo Jin Lee, Jiyoon Jung, Youngseok Lee, Nam Hee Won, Yang Seok Chae; J Pathol Transl Med. 2016;50(4):287-293. Published online June 13, 2016; DOI: https://doi.org/10.4132/jptm.2016.04.04

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Abstract PDF

Background
Atypia of undetermined significance (AUS) is a category that encompasses a heterogeneous group of thyroid aspiration cytology. It has been reclassified into two subgroups based on the cytomorphologic features: AUS with cytologic atypia and AUS with architectural atypia. The nuclear characteristics of AUS with cytologic atypia need to be clarified by comparing to those observed in Hashimoto thyroiditis and benign follicular lesions.
Methods
We selected 84 cases of AUS with histologic follow-up, 24 cases of Hashimoto thyroiditis, and 26 cases of benign follicular lesions. We also subcategorized the AUS group according to the follow-up biopsy results into a papillary carcinoma group and a nodular hyperplasia group. The differences in morphometric parameters, including the nuclear areas and perimeters, were compared between these groups.
Results
The AUS group had significantly smaller nuclear areas than the Hashimoto thyroiditis group, but the nuclear perimeters were not statistically different. The AUS group also had significantly smaller nuclear areas than the benign follicular lesion group; however, the AUS group had significantly longer nuclear perimeters. The nuclear areas in the papillary carcinoma group were significantly smaller than those in the nodular hyperplasia group; however, the nuclear perimeters were not statistically different.
Conclusions
We found the AUS group to be a heterogeneous entity, including histologic follow-up diagnoses of papillary carcinoma and nodular hyperplasia. The AUS group showed significantly greater nuclear irregularities than the other two groups. Utilizing these features, nuclear morphometry could lead to improvements in the accuracy of the subjective diagnoses made with thyroid aspiration cytology.

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Prema Saldanha
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Tarunpreet Saini, Reetu Kundu, Manish Rohilla, Parikshaa Gupta, Nalini Gupta, Radhika Srinivasan, Uma Nahar Saikia, Pranab Dey
Cytojournal.2024; 21: 38. CrossRef
Morphometric study in thyroid tumors
Iuliana Mohorea, Bogdan Socea, Alexandru Carâp, Dragoș Șerban, Zenaida Ceaușu, Mihail Ceaușu
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The Usefulness of Immunocytochemistry of CD56 in Determining Malignancy from Indeterminate Thyroid Fine-Needle Aspiration Cytology
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Clinical Significance of an HPV DNA Chip Test with Emphasis on HPV-16 and/or HPV-18 Detection in Korean Gynecological Patients: Min-Kyung Yeo, Ahwon Lee, Soo Young Hur, Jong Sup Park; J Pathol Transl Med. 2016;50(4):294-299. Published online June 26, 2016; DOI: https://doi.org/10.4132/jptm.2016.05.09

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Abstract PDF

Background
Human papillomavirus (HPV) is a major risk factor for cervical cancer.
Methods
We evaluated the clinical significance of the HPV DNA chip genotyping assay (MyHPV chip, Mygene Co.) compared with the Hybrid Capture 2 (HC2) chemiluminescent nucleic acid hybridization kit (Digene Corp.) in 867 patients.
Results
The concordance rate between the MyHPV chip and HC2 was 79.4% (kappa coefficient, κ = 0.55). The sensitivity and specificity of both HPV tests were very similar (approximately 85% and 50%, respectively). The addition of HPV result (either MyHPV chip or HC2) to cytology improved the sensitivity (95%, each) but reduced the specificity (approximately 30%, each) compared with the HPV test or cytology alone. Based on the MyHPV chip results, the odds ratio (OR) for ≥ high-grade squamous intraepithelial lesions (HSILs) was 9.9 in the HPV-16/18 (+) group and 3.7 in the non-16/18 high-risk (HR)-HPV (+) group. Based on the HC2 results, the OR for ≥ HSILs was 5.9 in the HR-HPV (+) group. When considering only patients with cytological diagnoses of “negative for intraepithelial lesion or malignancy” and “atypical squamous cell or atypical glandular cell,” based on the MyHPV chip results, the ORs for ≥ HSILs were 6.8 and 11.7, respectively, in the HPV-16/18 (+) group.
Conclusions
The sensitivity and specificity of the MyHPV chip test are similar to the HC2. Detecting HPV-16/18 with an HPV DNA chip test, which is commonly used in many Asian countries, is useful in assessing the risk of high-grade cervical lesions.

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Tina Shrestha, Won Choi, Ga Eon Kim, Jee Myung Yang, Kyung Chul Yoon
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Case Study

Isolated Mass-Forming IgG4-Related Cholangitis as an Initial Clinical Presentation of Systemic IgG4-Related Disease: Seokhwi Kim, Hyunsik Bae, Misun Choi, Binnari Kim, Jin Seok Heo, Ho Seong Kim, Seung Hee Choi, Kee-Taek Jang; J Pathol Transl Med. 2016;50(4):300-305. Published online January 11, 2016; DOI: https://doi.org/10.4132/jptm.2015.12.01

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IgG4-related disease (IgG4-RD) may involve multiple organs. Although it usually presents as diffuse organ involvement, localized mass-forming lesions have been occasionally encountered in pancreas. However, the same pattern has been seldom reported in biliary tract. A 61-year-old male showed a hilar bile duct mass with multiple enlarged lymph nodes in imaging studies and he underwent trisectionectomy under impression of cholangiocarcinoma. Gross examination revealed a mass-like lesion around hilar bile duct. Histopathologically, dense lymphoplasmacytic infiltration and storiform fibrosis were identified without evidence of malignancy. Immunohistochemical stain demonstrated rich IgG4-positive plasma cell infiltration. Follow-up imaging studies disclosed multiple enlarged lymph nodes with involvement of pancreas and perisplenic soft tissue. The lesions have been significantly reduced after steroid treatment, which suggests multi-organ involvement of systemic IgG4-RD. Here, we report an unusual localized mass-forming IgG4-related cholangitis as an initial presentation of IgG4-RD, which was biliary manifestation of systemic IgG4-related autoimmune disease.

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Retraction

Notice of Retraction: Therapeutic Effects of Umbilical Cord Blood Derived Mesenchymal Stem Cell-Conditioned Medium on Pulmonary Arterial Hypertension in Rats: Jae Chul Lee, Choong Ik Cha, Dong-Sik Kim, Soo Young Choe; J Pathol Transl Med. 2016;50(4):325-325. Published online July 15, 2016; DOI: https://doi.org/10.4132/jptm.2015.09.11.r; Retracts: J Pathol Transl Med 2015;49(6):472

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