TY - JOUR
T1 - Metabolomics and proteomics study reveals the effects of benzo[a]pyrene on the viability and migration of KYSE-150 esophageal cells
AU - Shen, Yuting
AU - Xie, Guangshan
AU - Lin, Siyi
AU - Zhu, Lin
AU - Zhang, Hongna
AU - Yang, Zhu
AU - Cai, Zongwei
N1 - Funding Information:
We gratefully acknowledge the funding support of the internal research funds SKLP_1920_P07 and RC-SGT2/18–19/SCI/008 from Hong Kong Baptist University , Hong Kong, China, and General Research Fund (GRF) 12103820 from the University Grants Committee (UGC), Hong Kong, China. The authors thank Prof. Zhaoxiang Bian, Dr. Cheng-yuan Lin, and Miss Siyi Lin of Hong Kong Baptist University for their kindly gifts of the cell lines KYSE-70, KYSE-150, and KYSE-450; Dr. Yanjun Hong of Sun Yat-sen University, Dr. Zhiyi Yang of Hong Kong Baptist University, and Dr. Xuan Li of the Shenzhen Center for Disease Control and Prevention for the gift of the KYSE-410 cell line; Dr. Yuanyuan Song and Miss Xiaoxiao Wang of Hong Kong Baptist University for their assistance and support in performing the omics analysis; and Dr. Simon Wang at the Language Center, Baptist University for help with editing the manuscript.
Funding Information:
We gratefully acknowledge the funding support of the internal research funds SKLP_1920_P07 and RC-SGT2/18?19/SCI/008 from Hong Kong Baptist University, Hong Kong, China, and General Research Fund (GRF) 12103820 from the University Grants Committee (UGC), Hong Kong, China. The authors thank Prof. Zhaoxiang Bian, Dr. Cheng-yuan Lin, and Miss Siyi Lin of Hong Kong Baptist University for their kindly gifts of the cell lines KYSE-70, KYSE-150, and KYSE-450; Dr. Yanjun Hong of Sun Yat-sen University, Dr. Zhiyi Yang of Hong Kong Baptist University, and Dr. Xuan Li of the Shenzhen Center for Disease Control and Prevention for the gift of the KYSE-410 cell line; Dr. Yuanyuan Song and Miss Xiaoxiao Wang of Hong Kong Baptist University for their assistance and support in performing the omics analysis; and Dr. Simon Wang at the Language Center, Baptist University for help with editing the manuscript.
Publisher Copyright:
© 2022 Elsevier B.V.
PY - 2022/6/10
Y1 - 2022/6/10
N2 - A representative polycyclic aromatic hydrocarbon, benzo[a]pyrene (B[a]P), has been widely detected in environmental compartments and is highly carcinogenic to humans. Oral ingestion of B[a]P is the dominant exposure pathway. The esophagus acts as the first contact point when B[a]P enters the human body. However, its role in the development of human esophageal cancer is rarely discussed. Herein, we employed untargeted metabolomics in combination with proteomics to explore B[a]P-related intracellular responses in human esophageal cell lines. Our results demonstrated that B[a]P exposure induced significant metabolic disorders, further leading to overproduction of reactive oxygen species (ROS) and disturbance of the cellular viability process and migration ability of esophageal cells. In response, glutathione (GSH) was consumed to meet the demand for cellular detoxification, and thioredoxin (TXN) was upregulated to balance the cellular redox. These alterations caused the reregulation of some specific protein families, including S100A proteins, ribosomal proteins, and histone H1 proteins. Such changes impeded the viability and migration of esophageal cells, which could adversely affect wound healing of the epithelium. These cellular responses indicate that B[a]P will cause serious cellular damage to esophageal cells and increase the carcinogenic risk even as a result of short-term exposure. Synopsis: Our omics study demonstrated how benzo[a]pyrene hampered the migration of esophageal cells and proposed a plausible mechanism underlying its carcinogenicity, which may contribute to our understanding of environmental pollutants.
AB - A representative polycyclic aromatic hydrocarbon, benzo[a]pyrene (B[a]P), has been widely detected in environmental compartments and is highly carcinogenic to humans. Oral ingestion of B[a]P is the dominant exposure pathway. The esophagus acts as the first contact point when B[a]P enters the human body. However, its role in the development of human esophageal cancer is rarely discussed. Herein, we employed untargeted metabolomics in combination with proteomics to explore B[a]P-related intracellular responses in human esophageal cell lines. Our results demonstrated that B[a]P exposure induced significant metabolic disorders, further leading to overproduction of reactive oxygen species (ROS) and disturbance of the cellular viability process and migration ability of esophageal cells. In response, glutathione (GSH) was consumed to meet the demand for cellular detoxification, and thioredoxin (TXN) was upregulated to balance the cellular redox. These alterations caused the reregulation of some specific protein families, including S100A proteins, ribosomal proteins, and histone H1 proteins. Such changes impeded the viability and migration of esophageal cells, which could adversely affect wound healing of the epithelium. These cellular responses indicate that B[a]P will cause serious cellular damage to esophageal cells and increase the carcinogenic risk even as a result of short-term exposure. Synopsis: Our omics study demonstrated how benzo[a]pyrene hampered the migration of esophageal cells and proposed a plausible mechanism underlying its carcinogenicity, which may contribute to our understanding of environmental pollutants.
KW - Benzo[a]pyrene
KW - Esophageal cancer
KW - Metabolomics
KW - Polycyclic aromatic hydrocarbon
KW - Proteomics
UR - http://www.scopus.com/inward/record.url?scp=85124617144&partnerID=8YFLogxK
U2 - 10.1016/j.scitotenv.2022.153761
DO - 10.1016/j.scitotenv.2022.153761
M3 - Journal article
C2 - 35151731
AN - SCOPUS:85124617144
SN - 0048-9697
VL - 824
JO - Science of the Total Environment
JF - Science of the Total Environment
M1 - 153761
ER -