Low-Dose IFNγ Induces Tumor Cell Stemness in Tumor Microenvironment of Non-Small Cell Lung Cancer
IFNγ is conventionally recognized as an inflammatory cytokine that plays a central role in antitumor immunity. Although it has been used clinically to treat a variety of malignancies, low levels of IFNγ in the tumor microenvironment (TME) increase the risk of tumor metastasis during immunotherapy. A...
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Published in | Cancer research (Chicago, Ill.) Vol. 79; no. 14; pp. 3737 - 3748 |
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Main Authors | , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
15.07.2019
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Abstract | IFNγ is conventionally recognized as an inflammatory cytokine that plays a central role in antitumor immunity. Although it has been used clinically to treat a variety of malignancies, low levels of IFNγ in the tumor microenvironment (TME) increase the risk of tumor metastasis during immunotherapy. Accumulating evidence suggests that IFNγ can induce cancer progression, yet the mechanisms underlying the controversial role of IFNγ in tumor development remain unclear. Here, we reveal a dose-dependent effect of IFNγ in inducing tumor stemness to accelerate cancer progression in patients with a variety of cancer types. Low levels of IFNγ endowed cancer stem-like properties via the intercellular adhesion molecule-1 (ICAM1)-PI3K-Akt-Notch1 axis, whereas high levels of IFNγ activated the JAK1-STAT1-caspase pathway to induce apoptosis in non-small cell lung cancer (NSCLC). Inhibition of ICAM1 abrogated the stem-like properties of NSCLC cells induced by the low dose of IFNγ both
and
. This study unveils the role of low levels of IFNγ in conferring tumor stemness and elucidates the distinct signaling pathways activated by IFNγ in a dose-dependent manner, thus providing new insights into cancer treatment, particularly for patients with low expression of IFNγ in the TME. SIGNIFICANCE: These findings reveal the dose-dependent effect of IFNγ in inducing tumor stemness and elucidate the distinct molecular mechanisms activated by IFNγ in a dose-dependent manner. |
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AbstractList | Abstract
IFNγ is conventionally recognized as an inflammatory cytokine that plays a central role in antitumor immunity. Although it has been used clinically to treat a variety of malignancies, low levels of IFNγ in the tumor microenvironment (TME) increase the risk of tumor metastasis during immunotherapy. Accumulating evidence suggests that IFNγ can induce cancer progression, yet the mechanisms underlying the controversial role of IFNγ in tumor development remain unclear. Here, we reveal a dose-dependent effect of IFNγ in inducing tumor stemness to accelerate cancer progression in patients with a variety of cancer types. Low levels of IFNγ endowed cancer stem-like properties via the intercellular adhesion molecule-1 (ICAM1)–PI3K–Akt–Notch1 axis, whereas high levels of IFNγ activated the JAK1–STAT1–caspase pathway to induce apoptosis in non–small cell lung cancer (NSCLC). Inhibition of ICAM1 abrogated the stem-like properties of NSCLC cells induced by the low dose of IFNγ both in vitro and in vivo. This study unveils the role of low levels of IFNγ in conferring tumor stemness and elucidates the distinct signaling pathways activated by IFNγ in a dose-dependent manner, thus providing new insights into cancer treatment, particularly for patients with low expression of IFNγ in the TME.
Significance:
These findings reveal the dose-dependent effect of IFNγ in inducing tumor stemness and elucidate the distinct molecular mechanisms activated by IFNγ in a dose-dependent manner. IFNγ is conventionally recognized as an inflammatory cytokine that plays a central role in antitumor immunity. Although it has been used clinically to treat a variety of malignancies, low levels of IFNγ in the tumor microenvironment (TME) increase the risk of tumor metastasis during immunotherapy. Accumulating evidence suggests that IFNγ can induce cancer progression, yet the mechanisms underlying the controversial role of IFNγ in tumor development remain unclear. Here, we reveal a dose-dependent effect of IFNγ in inducing tumor stemness to accelerate cancer progression in patients with a variety of cancer types. Low levels of IFNγ endowed cancer stem-like properties via the intercellular adhesion molecule-1 (ICAM1)-PI3K-Akt-Notch1 axis, whereas high levels of IFNγ activated the JAK1-STAT1-caspase pathway to induce apoptosis in non-small cell lung cancer (NSCLC). Inhibition of ICAM1 abrogated the stem-like properties of NSCLC cells induced by the low dose of IFNγ both and . This study unveils the role of low levels of IFNγ in conferring tumor stemness and elucidates the distinct signaling pathways activated by IFNγ in a dose-dependent manner, thus providing new insights into cancer treatment, particularly for patients with low expression of IFNγ in the TME. SIGNIFICANCE: These findings reveal the dose-dependent effect of IFNγ in inducing tumor stemness and elucidate the distinct molecular mechanisms activated by IFNγ in a dose-dependent manner. |
Author | Ping, Yu Liu, Shasha Wang, Liping Yang, Li Li, Feng Sun, Ting Cheng, Shaoyan Zhang, Yi Xia, Jianchuan Zhang, Kai Li, Zihai Qu, Jiao Yue, Dongli Zhang, Chaoqi Zhang, Bin Song, Mengjia Maimela, Nomathamsanqa Resegofetse |
Author_xml | – sequence: 1 givenname: Mengjia surname: Song fullname: Song, Mengjia organization: Department of Biotherapy, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 2 givenname: Yu surname: Ping fullname: Ping, Yu organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 3 givenname: Kai surname: Zhang fullname: Zhang, Kai organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 4 givenname: Li surname: Yang fullname: Yang, Li organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 5 givenname: Feng surname: Li fullname: Li, Feng organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 6 givenname: Chaoqi surname: Zhang fullname: Zhang, Chaoqi organization: Department of Thoracic Surgery, National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China – sequence: 7 givenname: Shaoyan surname: Cheng fullname: Cheng, Shaoyan organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 8 givenname: Dongli surname: Yue fullname: Yue, Dongli organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 9 givenname: Nomathamsanqa Resegofetse surname: Maimela fullname: Maimela, Nomathamsanqa Resegofetse organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 10 givenname: Jiao surname: Qu fullname: Qu, Jiao organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 11 givenname: Shasha surname: Liu fullname: Liu, Shasha organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 12 givenname: Ting surname: Sun fullname: Sun, Ting organization: Biotherapy Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China – sequence: 13 givenname: Zihai surname: Li fullname: Li, Zihai organization: Department of Microbiology and Immunology, Medical University of South Carolina, Charleston, South Carolina – sequence: 14 givenname: Jianchuan surname: Xia fullname: Xia, Jianchuan organization: Department of Biotherapy, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 15 givenname: Bin surname: Zhang fullname: Zhang, Bin organization: Division of Hematology/Oncology, Department of Medicine, Robert H. Lurie Comprehensive Cancer Center, Northwestern University Feinberg School of Medicine, Chicago, Illinois – sequence: 16 givenname: Liping surname: Wang fullname: Wang, Liping email: yizhang@zzu.edu.cn, wlp@zzu.edu.cn organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China. yizhang@zzu.edu.cn wlp@zzu.edu.cn – sequence: 17 givenname: Yi surname: Zhang fullname: Zhang, Yi email: yizhang@zzu.edu.cn, wlp@zzu.edu.cn organization: Cancer Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31085700$$D View this record in MEDLINE/PubMed |
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Snippet | IFNγ is conventionally recognized as an inflammatory cytokine that plays a central role in antitumor immunity. Although it has been used clinically to treat a... Abstract IFNγ is conventionally recognized as an inflammatory cytokine that plays a central role in antitumor immunity. Although it has been used clinically to... |
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SubjectTerms | A549 Cells Animals Apoptosis - drug effects Carcinoma, Non-Small-Cell Lung - drug therapy Carcinoma, Non-Small-Cell Lung - metabolism Carcinoma, Non-Small-Cell Lung - pathology Caspases - metabolism Cell Line, Tumor Dose-Response Relationship, Drug Female Humans Intercellular Adhesion Molecule-1 - metabolism Interferon-gamma - administration & dosage Janus Kinase 1 - metabolism Lung Neoplasms - drug therapy Lung Neoplasms - metabolism Lung Neoplasms - pathology Mice Mice, Inbred NOD Mice, SCID Neoplastic Stem Cells - drug effects Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Phosphatidylinositol 3-Kinases - metabolism Proto-Oncogene Proteins c-akt - metabolism Receptor, Notch1 - metabolism Recombinant Proteins - pharmacology Signal Transduction - drug effects STAT1 Transcription Factor - metabolism Tumor Microenvironment - drug effects Xenograft Model Antitumor Assays |
Title | Low-Dose IFNγ Induces Tumor Cell Stemness in Tumor Microenvironment of Non-Small Cell Lung Cancer |
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