Retrospective Study
Copyright ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Aug 21, 2020; 26(31): 4656-4668
Published online Aug 21, 2020. doi: 10.3748/wjg.v26.i31.4656
Clinical and prognostic significance of CC chemokine receptor type 8 protein expression in gastrointestinal stromal tumors
Huai-Liang Li, Lin-Hua Wang, Yi-Lin Hu, Ying Feng, Xiao-Hong Li, Yi-Fei Liu, Peng Li, Qin-Sheng Mao, Wan-Jiang Xue
Huai-Liang Li, Yi-Lin Hu, Ying Feng, Peng Li, Qin-Sheng Mao, Wan-Jiang Xue, Department of Gastrointestinal Surgery, Nantong University Affiliated Hospital, Nantong 226001, Jiangsu Province, China
Lin-Hua Wang, Department of Intensive Care Unit, Nantong University Affiliated Hospital, Nantong 226001, Jiangsu Province, China
Xiao-Hong Li, Department of Surgical Comprehensive Laboratory, Nantong University Affiliated Hospital, Nantong 226001, Jiangsu Province, China
Yi-Fei Liu, Department of Pathology, Nantong University Affiliated Hospital, Nantong 226001, Jiangsu Province, China
Author contributions: Li HL and Wang LH contributed equally to this work; Li HL wrote the paper; Wang LH performed the research; Hu YL contributed new reagents or analytic tools; Feng Y and Liu YF analyzed the data; Mao QS and Xue WJ edited the paper and provided primary revised opinion; Xue WJ designed the research.
Institutional review board statement: This study was reviewed and approved by the Ethics Committee of the Nantong University Affiliated Hospital.
Informed consent statement: Informed written consent was obtained from the patients for publication of this report and any accompanying images.
Conflict-of-interest statement: We have no financial relationships to disclose.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Wan-Jiang Xue, FAASLD, BSc, MD, PhD, Chief Doctor, Professor, Department of Gastrointestinal Surgery, Nantong University Affiliated Hospital, No. 20 Xisi Street, Nantong 226001, Jiangsu Province, China. xuewanjiang@ntu.edu.cn
Received: March 4, 2020
Peer-review started: March 4, 2020
First decision: April 25, 2020
Revised: June 7, 2020
Accepted: July 18, 2020
Article in press: July 18, 2020
Published online: August 21, 2020
Processing time: 170 Days and 5.3 Hours
ARTICLE HIGHLIGHTS
Research background

Gastrointestinal stromal tumors (GISTs) are the most common mesenchymal neoplasms of the gastrointestinal tract. Surgical resection remains the main treatment for GISTs. Unfortunately, more than 50% of patients eventually develop local recurrence or metastasis. Although imatinib is the standard first-line therapy for patients with metastatic or advanced GISTs, it cannot cure the disease. The prognosis of the advanced cases is not optimistic. CC chemokine receptor type 8 (CCR8) protein participates in regulation of immune responses. Recent studies on CCR8 in non-small cell lung cancer and colorectal cancer showed that it was highly expressed in tumor-infiltrating regulatory T cells and correlated with a poor prognosis. However, there are only a few references on the expression of CCR8 protein in gastrointestinal stromal tumors.

Research motivation

The following problems, which we need to solve urgently, are also the research motivation of this article: (1) The function of the CCR8 in tumor immunity; (2) The relationship between the CCR8 expression and GIST clinical data; and (3) The relationship between the prognosis of GIST and CCR8.

Research objectives

In this study, we examined the expression of CCR8 in GISTs by immuno-histochemistry to explore the clinical significance of GIST expression and its prognosis. Based on the STRING database, we predicted the potential immunological function of CCR8. This research will provide evidence and support for the diagnosis of GIST, prognostic evaluation and new tumor treatment targets.

Research methods

Tissue samples were used for the tissue microarray construction. The microarrays were then subjected to immunohistochemical analyses to detect CCR8 expression. Next, Kaplan–Meier analysis was utilized to calculate the survival rate of patients with complete follow-up data, and the potential prognostic value of CCR8 was evaluated by Cox regression analysis. Finally, a Gene Ontology/Kyoto Encyclopedia of Genes and Genomes single-gene enrichment chart of CCR8 was constructed using the STRING database.

Research results

CCR8-positive signals were detected as brown or brown-yellow particles by im-munohistochemistry located in the cytoplasm. Among 125 tissue samples, 74 had CCR8 high expression, and 51 had low or negative expression. Statistical analyses suggested CCR8 was significantly correlated with tumor size, mitotic index, AFIP-Miettinen risk classification and tumor location. Kaplan–Meier and multivariate analyses showed that patients with low or negative CCR8 expression, mitotic index < 5/high-power field and tumor diameter < 5 cm had a better prognosis. Based on the STRING database, CCR8 was significantly enriched in biological processes such as tumor immunity, T lymphocyte chemotaxis, migration and pathways like the nuclear factor-κB and tumor necrosis factor pathways as well as intestinal immune regulation networks.

Research conclusions

The expression of CCR8 protein in GISTs correlated with tumor size, mitotic index, AFIP-Miettinen risk classification. Each index suggested that the higher the degree of malignancy was associated with higher CCR8 expression. When compared with other factors (age, sex, tumor location, etc), there was no relationship with CCR8. CCR8 low expression was positively correlated with the survival of patients with GISTs, which has some implications for the prognosis of patients. CCR8 can be used as an independent factor to evaluate the prognosis of GISTs. CCR8 was significantly enriched in biological processes such as tumor immunity, T lymphocyte chemotaxis, migration and pathways like the nuclear factor-κB and tumor necrosis factor pathways as well as intestinal immune regulation networks. These will provide ideas for future research about the specific mechanism of CCR8 in tumor immunity.

Research perspectives

Tumor immunity is currently a hotspot in cancer research, and the chemokine ligand/receptor axis plays an important role in the tumor immune mechanism of which CCR8 is the most brilliant one. Meanwhile, more and more studies focus on the immunopathogenesis of gastrointestinal stromal tumors. However, data on the relationship between CCR8 and the pathogenesis and treatment of GIST still remains unclear. This article is only a preliminary exploration of the study of CCR8 in gastrointestinal stromal tumors. The specific immunological mechanism of CCR8 in gastrointestinal stromal tumors is worthy of further exploration. We believe CCR8 could be a potential therapeutic target of GISTs.