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Published in: Clinical and Translational Oncology 9/2014

01-09-2014 | Research Article

Cell origins and significance of IL-17 in malignant pleural effusion

Authors: Y. Gong, S. X. Chen, B. A. Gao, R. C. Yao, L. Guan

Published in: Clinical and Translational Oncology | Issue 9/2014

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Abstract

Purpose

T cells are dominant in the immune regulation of malignant pleural effusion (MPE). However, it is unclear about the role of IL-17+ T cells, particularly for IL-17+CD8+ Tc17 cells in antitumor immunity. This retrospective study is aimed at evaluating the prognostic significance of IL-17+ T cells in patients with MPE.

Methods

The frequency of IL-17+CD4+ Th17 and IL-17+CD8+ Tc17 cells in peripheral blood (PB), pleural fluids (PF), and tumor tissues in 24 patients undergoing thoracoscopy was determined by flow cytometry, immunohistochemistry, and ELISA. The association among the different measures was analyzed by Spearman’s correlation tests.

Results

The percentages of PF Th17 and Tc17 cells were significantly higher than those in the PB of MPE patients and healthy controls (p < 0.01). Analysis of Th17 and Tc17 cells in the tumor tissues indicated that the percentages of Th17 and Tc17 cells in the invading tumor edge were significantly higher than those in the non-tumor tissues and intra-tumor regions (p < 0.05). More importantly, the percentages of IL-17+ T cells were associated with prolonged survival of patients with MPE.

Conclusions

Both Th17 and Tc17 cells were involved in the tumor immunity against MPE. Increased frequency of Tc17 cells may serve as a biomarker for the prognosis of patients with MPE.
Literature
1.
go back to reference Hu Y, Zhong Q. Basis of estimating pleural effusion size on CT scan: reasonable grouping of volume percentage. Chest. 2013;143:1839.PubMedCrossRef Hu Y, Zhong Q. Basis of estimating pleural effusion size on CT scan: reasonable grouping of volume percentage. Chest. 2013;143:1839.PubMedCrossRef
2.
go back to reference Bosch DJ, Muijs CT, Mul VE, Beukema JC, Hospers GA, Burgerhof JG, et al. Impact of neoadjuvant chemoradiotherapy on postoperative course after curative-intent transthoracic esophagectomy in esophageal cancer patients. Ann Surg Oncol. 2013. doi:10.1245/s10434-013-3316-8. Bosch DJ, Muijs CT, Mul VE, Beukema JC, Hospers GA, Burgerhof JG, et al. Impact of neoadjuvant chemoradiotherapy on postoperative course after curative-intent transthoracic esophagectomy in esophageal cancer patients. Ann Surg Oncol. 2013. doi:10.​1245/​s10434-013-3316-8.
3.
go back to reference Xu CH, Zhan P, Yu LK, Zhang XW. Diagnostic value of pleural interleukin 17 and carcinoembryonic antigen in lung cancer patients with malignant pleural effusions. Tumour Biol J Int Soc Codev Biol Med. 2013. doi:10.1007/s13277-013-1220-2. Xu CH, Zhan P, Yu LK, Zhang XW. Diagnostic value of pleural interleukin 17 and carcinoembryonic antigen in lung cancer patients with malignant pleural effusions. Tumour Biol J Int Soc Codev Biol Med. 2013. doi:10.​1007/​s13277-013-1220-2.
4.
go back to reference Johnson BE, Kabbinavar F, Fehrenbacher L, Hainsworth J, Kasubhai S, Kressel B, et al. ATLAS: randomized, double-blind, placebo-controlled, phase IIIB trial comparing bevacizumab therapy with or without erlotinib, after completion of chemotherapy, with bevacizumab for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol Off J Am Soc Clin Oncol. 2013;31:3926–35. Johnson BE, Kabbinavar F, Fehrenbacher L, Hainsworth J, Kasubhai S, Kressel B, et al. ATLAS: randomized, double-blind, placebo-controlled, phase IIIB trial comparing bevacizumab therapy with or without erlotinib, after completion of chemotherapy, with bevacizumab for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol Off J Am Soc Clin Oncol. 2013;31:3926–35.
5.
go back to reference Yang WB, Ye ZJ, Xiang F, Zhang JC, Zhou Q. Th17/Treg imbalance in malignant pleural effusion. Journal of Huazhong University of Science and Technology. Medical sciences = Hua zhong ke ji da xue xue bao. Yi xue Ying De wen ban = Huazhong keji daxue xuebao. Yixue Yingdewen ban. 2013;33:27–32. Yang WB, Ye ZJ, Xiang F, Zhang JC, Zhou Q. Th17/Treg imbalance in malignant pleural effusion. Journal of Huazhong University of Science and Technology. Medical sciences = Hua zhong ke ji da xue xue bao. Yi xue Ying De wen ban = Huazhong keji daxue xuebao. Yixue Yingdewen ban. 2013;33:27–32.
6.
go back to reference Kumawat AK, Strid H, Tysk C, Bohr J, Hornquist EH. Microscopic colitis patients demonstrate a mixed Th17/Tc17 and Th1/Tc1 mucosal cytokine profile. Mol Immunol. 2013;55:355–64.PubMedCrossRef Kumawat AK, Strid H, Tysk C, Bohr J, Hornquist EH. Microscopic colitis patients demonstrate a mixed Th17/Tc17 and Th1/Tc1 mucosal cytokine profile. Mol Immunol. 2013;55:355–64.PubMedCrossRef
7.
go back to reference Yang WB, Liang QL, Ye ZJ, Niu CM, Ma WL, Xiong XZ, et al. Cell origins and diagnostic accuracy of interleukin 27 in pleural effusions. PLoS ONE. 2012;7:e40450.PubMedCentralPubMedCrossRef Yang WB, Liang QL, Ye ZJ, Niu CM, Ma WL, Xiong XZ, et al. Cell origins and diagnostic accuracy of interleukin 27 in pleural effusions. PLoS ONE. 2012;7:e40450.PubMedCentralPubMedCrossRef
8.
go back to reference Ye ZJ, Zhou Q, Zhang JC, Li X, Wu C, Qin SM, et al. CD39+ regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a LAP-dependent mechanism. Respir Res. 2011;12:77.PubMedCentralPubMedCrossRef Ye ZJ, Zhou Q, Zhang JC, Li X, Wu C, Qin SM, et al. CD39+ regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a LAP-dependent mechanism. Respir Res. 2011;12:77.PubMedCentralPubMedCrossRef
9.
go back to reference Ghirelli C, Hagemann T. Targeting immunosuppression for cancer therapy. J Clin Investig. 2013;123:1–3.CrossRef Ghirelli C, Hagemann T. Targeting immunosuppression for cancer therapy. J Clin Investig. 2013;123:1–3.CrossRef
10.
go back to reference Kawakami Y, Yaguchi T, Sumimoto H, Kudo-Saito C, Tsukamoto N, Iwata-Kajihara T, et al. Cancer-induced immunosuppressive cascades and their reversal by molecular-targeted therapy. Ann NY Acad Sci. 2013;1284:80–6.PubMedCrossRef Kawakami Y, Yaguchi T, Sumimoto H, Kudo-Saito C, Tsukamoto N, Iwata-Kajihara T, et al. Cancer-induced immunosuppressive cascades and their reversal by molecular-targeted therapy. Ann NY Acad Sci. 2013;1284:80–6.PubMedCrossRef
11.
go back to reference Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457:102–6.PubMedCentralPubMedCrossRef Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457:102–6.PubMedCentralPubMedCrossRef
12.
go back to reference Altomare E, Fallarini S, Biaggi G, Gattoni E, Botta M, Lombardi G. Increased frequency of circulating invariant natural killer T cells in malignant pleural mesothelioma patients. Cancer Biol Ther. 2012;13:702–11.PubMedCrossRef Altomare E, Fallarini S, Biaggi G, Gattoni E, Botta M, Lombardi G. Increased frequency of circulating invariant natural killer T cells in malignant pleural mesothelioma patients. Cancer Biol Ther. 2012;13:702–11.PubMedCrossRef
13.
go back to reference Penido C, Castro-Faria-Neto HC, Larangeira AP, Rosas EC, Ribeiro-dos-Santos R, Bozza PT, et al. The role of gammadelta T lymphocytes in lipopolysaccharide-induced eosinophil accumulation into the mouse pleural cavity. J Immunol. 1997;159:853–60.PubMed Penido C, Castro-Faria-Neto HC, Larangeira AP, Rosas EC, Ribeiro-dos-Santos R, Bozza PT, et al. The role of gammadelta T lymphocytes in lipopolysaccharide-induced eosinophil accumulation into the mouse pleural cavity. J Immunol. 1997;159:853–60.PubMed
14.
go back to reference Suzuki E, Kapoor V, Cheung HK, Ling LE, DeLong PA, Kaiser LR, et al. Soluble type II transforming growth factor-beta receptor inhibits established murine malignant mesothelioma tumor growth by augmenting host antitumor immunity. Clinical cancer research: an official journal of the American Association for. Cancer Res. 2004;10:5907–18. Suzuki E, Kapoor V, Cheung HK, Ling LE, DeLong PA, Kaiser LR, et al. Soluble type II transforming growth factor-beta receptor inhibits established murine malignant mesothelioma tumor growth by augmenting host antitumor immunity. Clinical cancer research: an official journal of the American Association for. Cancer Res. 2004;10:5907–18.
15.
go back to reference Larypoor M, Bayat M, Zuhair MH, Akhavan Sepahy A, Amanlou M. Evaluation of the number of CD4(+) CD25(+) FoxP3(+) Treg cells in normal mice exposed to AFB1 and treated with aged garlic extract. Cell J. 2013;15:37–44.PubMedCentralPubMed Larypoor M, Bayat M, Zuhair MH, Akhavan Sepahy A, Amanlou M. Evaluation of the number of CD4(+) CD25(+) FoxP3(+) Treg cells in normal mice exposed to AFB1 and treated with aged garlic extract. Cell J. 2013;15:37–44.PubMedCentralPubMed
16.
go back to reference Richert L, Hue S, Hocini H, Raimbault M, Lacabaratz C, Surenaud M, et al. Cytokine and gene transcription profiles of immune responses elicited by HIV lipopeptide vaccine in HIV-negative volunteers. AIDS (London, England). 2013;27:1421–31.CrossRef Richert L, Hue S, Hocini H, Raimbault M, Lacabaratz C, Surenaud M, et al. Cytokine and gene transcription profiles of immune responses elicited by HIV lipopeptide vaccine in HIV-negative volunteers. AIDS (London, England). 2013;27:1421–31.CrossRef
17.
go back to reference Zhang C, Gui L, Xu Y, Wu T, Liu D. Preventive effects of andrographolide on the development of diabetes in autoimmune diabetic NOD mice by inducing immune tolerance. Int Immunopharmacol. 2013;16:451–6.PubMedCrossRef Zhang C, Gui L, Xu Y, Wu T, Liu D. Preventive effects of andrographolide on the development of diabetes in autoimmune diabetic NOD mice by inducing immune tolerance. Int Immunopharmacol. 2013;16:451–6.PubMedCrossRef
18.
go back to reference Ye ZJ, Zhou Q, Gu YY, Qin SM, Ma WL, Xin JB, et al. Generation and differentiation of IL-17-producing CD4+ T cells in malignant pleural effusion. J Immunol. 2010;185:6348–54.PubMedCrossRef Ye ZJ, Zhou Q, Gu YY, Qin SM, Ma WL, Xin JB, et al. Generation and differentiation of IL-17-producing CD4+ T cells in malignant pleural effusion. J Immunol. 2010;185:6348–54.PubMedCrossRef
19.
go back to reference Jain A, Pandey N, Garg RK, Kumar R. IL-17 level in patients with Dengue virus infection and its association with severity of illness. J Clin Immunol. 2013;33:613–8.PubMedCrossRef Jain A, Pandey N, Garg RK, Kumar R. IL-17 level in patients with Dengue virus infection and its association with severity of illness. J Clin Immunol. 2013;33:613–8.PubMedCrossRef
20.
go back to reference Li X, Zhou Q, Yang WB, Xiong XZ, Du RH, Zhang JC. Pleural mesothelial cells promote expansion of IL-17-producing CD8+ T cells in tuberculous pleural effusion. J Clin Immunol. 2013;33:775–87.PubMedCrossRef Li X, Zhou Q, Yang WB, Xiong XZ, Du RH, Zhang JC. Pleural mesothelial cells promote expansion of IL-17-producing CD8+ T cells in tuberculous pleural effusion. J Clin Immunol. 2013;33:775–87.PubMedCrossRef
Metadata
Title
Cell origins and significance of IL-17 in malignant pleural effusion
Authors
Y. Gong
S. X. Chen
B. A. Gao
R. C. Yao
L. Guan
Publication date
01-09-2014
Publisher
Springer Milan
Published in
Clinical and Translational Oncology / Issue 9/2014
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-013-1152-8

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