IL‐10 derived from M2 macrophage promotes cancer stemness via JAK1/STAT1/NF‐κB/Notch1 pathway in non‐small cell lung cancer

Yang, Li; Dong, Ying; Li, Yanjun; Wang, Dong; Liu, Shasha; Wang, Dan; Gao, Qun; Ji, Shaofei; Chen, Xinfeng; Lei, Qingyang; Jiang, Wenyi; Wang, Liping; Zhang, Bin; Yu, Jane J.; Zhang, Yi

doi:10.1002/ijc.32151

Title: IL‐10 derived from M2 macrophage promotes cancer stemness via JAK1/STAT1/NF‐κB/Notch1 pathway in non‐small cell lung cancer

Journal Article · 06 February 2019 · International Journal of Cancer

DOI: https://doi.org/10.1002/ijc.32151 · OSTI ID:1493929

Yang, Li ^[1]; Dong, Ying ^[1]; Li, Yanjun ^[2]; Wang, Dong ^[1]; Liu, Shasha ^[2]; Wang, Dan ^[1]; Gao, Qun ^[1]; Ji, Shaofei ^[3]; Chen, Xinfeng ^[1]; Lei, Qingyang ^[1]; Jiang, Wenyi ^[1]; Wang, Liping ^[4]; Zhang, Bin ^[5]; Yu, Jane J. ^[6];

^[7]

Biotherapy Center The First Affiliated Hospital of Zhengzhou University Zhengzhou Henan People's Republic of China, Department of Oncology The First Affiliated Hospital of Zhengzhou University Zhengzhou Henan People's Republic of China, Key Laboratory for Tumor Immunology and Biotherapy of Henan Province Zhengzhou Henan People's Republic of China
Biotherapy Center The First Affiliated Hospital of Zhengzhou University Zhengzhou Henan People's Republic of China, Key Laboratory for Tumor Immunology and Biotherapy of Henan Province Zhengzhou Henan People's Republic of China, School of Life Sciences Zhengzhou University Zhengzhou Henan People's Republic of China
Department of Radiology Orthopaedic Hospital of Zhengzhou City Zhengzhou Henan People's Republic of China
Department of Oncology The First Affiliated Hospital of Zhengzhou University Zhengzhou Henan People's Republic of China, Key Laboratory for Tumor Immunology and Biotherapy of Henan Province Zhengzhou Henan People's Republic of China
Department of Hematology/Oncology, School of Medicine Northwestern University Chicago IL
Division of Pulmonary, Critical Care and Sleep Medicine, Department of Internal Medicine, College of Medicine University of Cincinnati Cincinnati OH
Biotherapy Center The First Affiliated Hospital of Zhengzhou University Zhengzhou Henan People's Republic of China, Department of Oncology The First Affiliated Hospital of Zhengzhou University Zhengzhou Henan People's Republic of China, Key Laboratory for Tumor Immunology and Biotherapy of Henan Province Zhengzhou Henan People's Republic of China, School of Life Sciences Zhengzhou University Zhengzhou Henan People's Republic of China

Tumor‐associated macrophages (TAMs), key immune cells in the tumor microenvironment, are shown to be closely correlated with the progression of non‐small cell lung cancer (NSCLC). Cancer stem cells (CSCs) can contribute to NSCLC progression as well. We aimed to clarify whether TAMs promote the progression of NSCLC by mainly affecting the activities of CSCs. We found that TAM‐like cells promoted CSC‐like properties in NSCLC cells in vitro , which was mediated by TAM‐derived IL‐10. TAM‐derived IL‐10 promoted CSC‐like properties of NSCLC cells through JAK1/STAT1/NF‐κB/Notch1 signaling. Blockade of IL‐10/JAK1 signaling inhibited TAM‐mediated NSCLC tumor growth in vivo , and the TAM‐mediated expression of CSC‐related and mesenchymal‐related genes in NSCLC. Lastly, expression levels of these signaling molecules were significantly correlated with survival of NSCLC patients. Therefore, IL‐10/JAK1 signaling might be a potential therapeutic target for NSCLC treatment.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1493929

Journal Information:: International Journal of Cancer, Journal Name: International Journal of Cancer Journal Issue: 4 Vol. 145; ISSN 0020-7136

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United States

Language:: English

References (40)

Baricitinib, Methotrexate, or Combination in Patients With Rheumatoid Arthritis and No or Limited Prior Disease-Modifying Antirheumatic Drug Treatment: BARICITINIB IN PATIENTS WITH EARLY RHEUMATOID ARTHRITIS Fleischmann, Roy; Schiff, Michael; van der Heijde, Désirée Arthritis & Rheumatology, Vol. 69, Issue 3 https://doi.org/10.1002/art.39953	journal	February 2017
International lung cancer trends by histologic type: Male:Female differences diminishing and adenocarcinoma rates rising Devesa, Susan S.; Bray, Freddie; Vizcaino, A. Paloma International Journal of Cancer, Vol. 117, Issue 2 https://doi.org/10.1002/ijc.21183	journal	January 2005
Impaired T cell function in malignant pleural effusion is caused by TGF-β derived predominantly from macrophages: Impaired T Cell Function in Malignant Pleural Effusion Li, Lifeng; Yang, Li; Wang, Liping International Journal of Cancer, Vol. 139, Issue 10 https://doi.org/10.1002/ijc.30289	journal	August 2016
Tumor-Associated Macrophages Regulate Murine Breast Cancer Stem Cells Through a Novel Paracrine EGFR/Stat3/Sox-2 Signaling Pathway Yang, Jian; Liao, Debbie; Chen, Cong STEM CELLS, Vol. 31, Issue 2 https://doi.org/10.1002/stem.1281	journal	February 2013
CD163+CD14+ macrophages, a potential immune biomarker for malignant pleural effusion Wang, Fei; Yang, Li; Gao, Qun Cancer Immunology, Immunotherapy, Vol. 64, Issue 8 https://doi.org/10.1007/s00262-015-1701-9	journal	May 2015
Down-regulation of JAK1 by RNA interference inhibits growth of the lung cancer cell line A549 and interferes with the PI3K/mTOR pathway Liu, Dan; Huang, Yi; Zeng, Jing Journal of Cancer Research and Clinical Oncology, Vol. 137, Issue 11 https://doi.org/10.1007/s00432-011-1037-6	journal	August 2011
Macrophages and Therapeutic Resistance in Cancer Ruffell, Brian; Coussens, Lisa M. Cancer Cell, Vol. 27, Issue 4 https://doi.org/10.1016/j.ccell.2015.02.015	journal	April 2015
Cancer Stem Cells: Impact, Heterogeneity, and Uncertainty Magee, Jeffrey A.; Piskounova, Elena; Morrison, Sean J. Cancer Cell, Vol. 21, Issue 3 https://doi.org/10.1016/j.ccr.2012.03.003	journal	March 2012
Targeting Tumor-Associated Macrophages with Anti-CSF-1R Antibody Reveals a Strategy for Cancer Therapy Ries, Carola H.; Cannarile, Michael A.; Hoves, Sabine Cancer Cell, Vol. 25, Issue 6 https://doi.org/10.1016/j.ccr.2014.05.016	journal	June 2014
IL-10 signalling blockade at the time of immunization inhibits Human papillomavirus 16 E7 transformed TC-1 tumour cells growth in mice Chen, Shu; Wang, Xiongfei; Wu, Xiaolian Cellular Immunology, Vol. 290, Issue 1 https://doi.org/10.1016/j.cellimm.2014.06.002	journal	July 2014
Temporary elimination of IL-10 enhanced the effectiveness of cyclophosphamide and BMDC-based therapy by decrease of the suppressor activity of MDSCs and activation of antitumour immune response Rossowska, Joanna; Anger, Natalia; Kicielińska, Jagoda Immunobiology, Vol. 220, Issue 3 https://doi.org/10.1016/j.imbio.2014.10.009	journal	March 2015
Tumor-Associated Macrophages: From Mechanisms to Therapy Noy, Roy; Pollard, Jeffrey W. Immunity, Vol. 41, Issue 1 https://doi.org/10.1016/j.immuni.2014.06.010	journal	July 2014
Molecular Profiling Reveals a Tumor-Promoting Phenotype of Monocytes and Macrophages in Human Cancer Progression Chittezhath, Manesh; Dhillon, Manprit Kaur; Lim, Jyue Yuan Immunity, Vol. 41, Issue 5 https://doi.org/10.1016/j.immuni.2014.09.014	journal	November 2014
Differential macrophage programming in the tumor microenvironment Ruffell, Brian; Affara, Nesrine I.; Coussens, Lisa M. Trends in Immunology, Vol. 33, Issue 3 https://doi.org/10.1016/j.it.2011.12.001	journal	March 2012
Nodal/Activin Signaling Drives Self-Renewal and Tumorigenicity of Pancreatic Cancer Stem Cells and Provides a Target for Combined Drug Therapy Lonardo, Enza; Hermann, Patrick C.; Mueller, Maria-Theresa Cell Stem Cell, Vol. 9, Issue 5 https://doi.org/10.1016/j.stem.2011.10.001	journal	November 2011
Hostile Takeover: Glioma Stem Cells Recruit TAMs to Support Tumor Progression Shi, Yu; Ping, Yi-fang; Zhang, Xia Cell Stem Cell, Vol. 16, Issue 3 https://doi.org/10.1016/j.stem.2015.02.008	journal	March 2015
The elegance of a macrophage De Santis, Maria; Locati, Massimo; Selmi, Carlo Cellular & Molecular Immunology, Vol. 15, Issue 3 https://doi.org/10.1038/cmi.2017.64	journal	July 2017
Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease Boulter, Luke; Govaere, Olivier; Bird, Tom G. Nature Medicine, Vol. 18, Issue 4 https://doi.org/10.1038/nm.2667	journal	March 2012
Cancer stem cells and tumor-associated macrophages: a roadmap for multitargeting strategies Raggi, C.; Mousa, H. S.; Correnti, M. Oncogene, Vol. 35, Issue 6 https://doi.org/10.1038/onc.2015.132	journal	May 2015
Homoharringtonine induces apoptosis and inhibits STAT3 via IL-6/JAK1/STAT3 signal pathway in Gefitinib-resistant lung cancer cells Cao, Wei; Liu, Ying; Zhang, Ran Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08477	journal	July 2015
The Role of CSF‐1 in Normal and Neoplastic Breast Physiology Sapi, Eva; Kacinski, Barry M. Proceedings of the Society for Experimental Biology and Medicine, Vol. 220, Issue 1 https://doi.org/10.1046/j.1525-1373.1999.d01-1.x	journal	January 1999
Tumor-Associated Macrophages Produce Interleukin 6 and Signal via STAT3 to Promote Expansion of Human Hepatocellular Carcinoma Stem Cells Wan, Shanshan; Zhao, Ende; Kryczek, Ilona Gastroenterology, Vol. 147, Issue 6 https://doi.org/10.1053/j.gastro.2014.08.039	journal	December 2014
Tumor-associated macrophages regulate tumorigenicity and anticancer drug responses of cancer stem/initiating cells Jinushi, M.; Chiba, S.; Yoshiyama, H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 30 https://doi.org/10.1073/pnas.1106645108	journal	July 2011
Anti-IL-10–mediated Enhancement of Antitumor Efficacy of a Dendritic Cell–targeting MIP3α-gp100 Vaccine in the B16F10 Mouse Melanoma Model Is Dependent on Type I Interferons Gordy, James T.; Luo, Kun; Francica, Brian Journal of Immunotherapy, Vol. 41, Issue 4 https://doi.org/10.1097/CJI.0000000000000212	journal	January 2018
Trends in Stage Distribution for Patients with Non-small Cell Lung Cancer: A National Cancer Database Survey Morgensztern, Daniel; Ng, Shean Huey; Gao, Feng Journal of Thoracic Oncology, Vol. 5, Issue 1 https://doi.org/10.1097/JTO.0b013e3181c5920c	journal	January 2010
Preclinical Profile of a Potent -Secretase Inhibitor Targeting Notch Signaling with In vivo Efficacy and Pharmacodynamic Properties Luistro, L.; He, W.; Smith, M. Cancer Research, Vol. 69, Issue 19 https://doi.org/10.1158/0008-5472.CAN-09-1843	journal	September 2009
Breast Cancer Stem Cells Are Regulated by Mesenchymal Stem Cells through Cytokine Networks Liu, Suling; Ginestier, Christophe; Ou, Sing J. Cancer Research, Vol. 71, Issue 2 https://doi.org/10.1158/0008-5472.CAN-10-0538	journal	January 2011
Targeting Tumor-Infiltrating Macrophages Decreases Tumor-Initiating Cells, Relieves Immunosuppression, and Improves Chemotherapeutic Responses Mitchem, J. B.; Brennan, D. J.; Knolhoff, B. L. Cancer Research, Vol. 73, Issue 3 https://doi.org/10.1158/0008-5472.CAN-12-2731	journal	December 2012
Metastasis Suppressors Regulate the Tumor Microenvironment by Blocking Recruitment of Prometastatic Tumor-Associated Macrophages Frankenberger, C.; Rabe, D.; Bainer, R. Cancer Research, Vol. 75, Issue 19 https://doi.org/10.1158/0008-5472.CAN-14-3394	journal	August 2015
Tumor Microenvironment of Metastasis in Human Breast Carcinoma: A Potential Prognostic Marker Linked to Hematogenous Dissemination Robinson, B. D.; Sica, G. L.; Liu, Y. -F. Clinical Cancer Research, Vol. 15, Issue 7 https://doi.org/10.1158/1078-0432.CCR-08-2179	journal	March 2009
A Phase I First-in-Human Study of Enoticumab (REGN421), a Fully Human Delta-like Ligand 4 (Dll4) Monoclonal Antibody in Patients with Advanced Solid Tumors Chiorean, E. G.; LoRusso, P.; Strother, R. M. Clinical Cancer Research, Vol. 21, Issue 12 https://doi.org/10.1158/1078-0432.CCR-14-2797	journal	February 2015
RAD51 Mediates Resistance of Cancer Stem Cells to PARP Inhibition in Triple-Negative Breast Cancer Liu, Yajing; Burness, Monika L.; Martin-Trevino, Rachel Clinical Cancer Research, Vol. 23, Issue 2 https://doi.org/10.1158/1078-0432.CCR-15-1348	journal	December 2016
Role of the Microenvironment in Liver Metastasis: From Pre- to Prometastatic Niches Brodt, P. Clinical Cancer Research, Vol. 22, Issue 24 https://doi.org/10.1158/1078-0432.CCR-16-0460	journal	October 2016
Activation of IL-6R/JAK1/STAT3 Signaling Induces De Novo Resistance to Irreversible EGFR Inhibitors in Non-Small Cell Lung Cancer with T790M Resistance Mutation Kim, S. M.; Kwon, O. -J.; Hong, Y. K. Molecular Cancer Therapeutics, Vol. 11, Issue 10 https://doi.org/10.1158/1535-7163.MCT-12-0311	journal	August 2012
Role of KEAP1 / NRF2 and TP53 Mutations in Lung Squamous Cell Carcinoma Development and Radiation Resistance Jeong, Youngtae; Hoang, Ngoc T.; Lovejoy, Alexander Cancer Discovery, Vol. 7, Issue 1 https://doi.org/10.1158/2159-8290.CD-16-0127	journal	September 2016
Tumor-associated macrophages: from basic research to clinical application Yang, Li; Zhang, Yi Journal of Hematology & Oncology, Vol. 10, Issue 1 https://doi.org/10.1186/s13045-017-0430-2	journal	February 2017
CD163+ tumor-associated macrophage is a prognostic biomarker and is associated with therapeutic effect on malignant pleural effusion of lung cancer patients Yang, Li; Wang, Fei; Wang, Liping Oncotarget, Vol. 6, Issue 12 https://doi.org/10.18632/oncotarget.3547	journal	March 2015
Rationally Repurposing Ruxolitinib (Jakafi®) as a Solid Tumor Therapeutic Tavallai, Mehrad; Booth, Laurence; Roberts, Jane L. Frontiers in Oncology, Vol. 6 https://doi.org/10.3389/fonc.2016.00142	journal	June 2016
1-O-acetylbritannilactone combined with gemcitabine elicits growth inhibition and apoptosis in A549 human non-small cell lung cancer cells Wang, Feng; Li, Hong; Qiao, Jian-Ou Molecular Medicine Reports, Vol. 12, Issue 4 https://doi.org/10.3892/mmr.2015.4042	journal	July 2015
Correlation of EGFR Del 19 with Fn14/JAK/STAT signaling molecules in non-small cell lung cancer Sun, Ying; Han, Yong; Wang, Xiaoping Oncology Reports, Vol. 36, Issue 2 https://doi.org/10.3892/or.2016.4905	journal	June 2016

Similar Records

STAT1 activation represses IL-22 gene expression and psoriasis pathogenesis

Journal Article · 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23125108

Bai, Li; Fang, Huihui; Xia, Sisi; +5 more

Long non-coding RNA GClnc1 knockdown suppresses progression of epithelial ovarian cancer by recruiting FOXC2 to disrupt the NOTCH1/NF-κB/Snail pathway

Journal Article · 2021 · Experimental Cell Research · OSTI ID:23195382

Wu, Dandan; Ke, Yumin; Xiao, Rongrong; +3 more

Celastrol inhibits cancer metastasis by suppressing M2-like polarization of macrophages

Journal Article · 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23105629

Yang, Yuening; Cheng, Shuyuan; Liang, Guikai; +2 more

Title: IL‐10 derived from M2 macrophage promotes cancer stemness via JAK1/STAT1/NF‐κB/Notch1 pathway in non‐small cell lung cancer

Citation Formats

References (40)

Similar Records

Related Subjects