Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma

Abstract Background Gliomas are the most common aggressive cancer in the central nervous system. Considering the difficulty in monitoring glioma response and progression, an approach is needed to evaluate the progression or survival of patients with glioma. We propose an application to facilitate cl...

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Autores principales: Wen Zhang, Tiancheng Qin, Zhenrong Yang, Liyuan Yin, Changyun Zhao, Lin Feng, Song Lin, Binlei Liu, Shujun Cheng, Kaitai Zhang
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Publicado: BMC 2021
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spelling oai:doaj.org-article:3f9330ab146a4664a2e90a634a1500f32021-11-14T12:17:04ZTelomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma10.1186/s12916-021-02138-71741-7015https://doaj.org/article/3f9330ab146a4664a2e90a634a1500f32021-11-01T00:00:00Zhttps://doi.org/10.1186/s12916-021-02138-7https://doaj.org/toc/1741-7015Abstract Background Gliomas are the most common aggressive cancer in the central nervous system. Considering the difficulty in monitoring glioma response and progression, an approach is needed to evaluate the progression or survival of patients with glioma. We propose an application to facilitate clinical detection and treatment monitoring in glioma patients by using telomerase-positive circulating tumor cells (CTCs) and to further evaluate the relationship between the immune microenvironment and CTCs in glioma patients. Methods From October 2014 to June 2017, 106 patients newly diagnosed with glioma were enrolled. We used the telomerase reverse transcriptase CTC detection method to detect and analyze the CTC statuses of glioma patients before and after surgery. FlowSight and FISH confirmed the CTCs detected by the telomerase-based method. To verify the correlation between CTCs and the immune response, peripheral white blood cell RNA sequencing was performed. Results CTCs were common in the peripheral blood of glioma patients and were not correlated with the pathological classification or grade of patients. The results showed that the presence of postoperative CTCs but not preoperative CTCs in glioma patients was a poor prognostic factor. The level of postoperative CTCs, which predicts a poor prognosis after surgery, may be associated with neutrophils. RNA sequencing suggested that postoperative CTCs were positively correlated with innate immune responses, especially the activation of neutrophils and the generation of neutrophil extracellular traps, but negatively correlated with the cytotoxic response. Conclusions Our results showed that telomerase-positive CTCs can predict a poor prognosis of patients with glioma. Our results also showed a correlation between CTCs and the immune macroenvironment, which provides a new perspective for the treatment of glioma.Wen ZhangTiancheng QinZhenrong YangLiyuan YinChangyun ZhaoLin FengSong LinBinlei LiuShujun ChengKaitai ZhangBMCarticleCirculating tumor cellsTelomerasePrognosisGliomaNeutrophilsImmune macroenvironmentMedicineRENBMC Medicine, Vol 19, Iss 1, Pp 1-16 (2021)
institution DOAJ
collection DOAJ
language EN
topic Circulating tumor cells
Telomerase
Prognosis
Glioma
Neutrophils
Immune macroenvironment
Medicine
R
spellingShingle Circulating tumor cells
Telomerase
Prognosis
Glioma
Neutrophils
Immune macroenvironment
Medicine
R
Wen Zhang
Tiancheng Qin
Zhenrong Yang
Liyuan Yin
Changyun Zhao
Lin Feng
Song Lin
Binlei Liu
Shujun Cheng
Kaitai Zhang
Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
description Abstract Background Gliomas are the most common aggressive cancer in the central nervous system. Considering the difficulty in monitoring glioma response and progression, an approach is needed to evaluate the progression or survival of patients with glioma. We propose an application to facilitate clinical detection and treatment monitoring in glioma patients by using telomerase-positive circulating tumor cells (CTCs) and to further evaluate the relationship between the immune microenvironment and CTCs in glioma patients. Methods From October 2014 to June 2017, 106 patients newly diagnosed with glioma were enrolled. We used the telomerase reverse transcriptase CTC detection method to detect and analyze the CTC statuses of glioma patients before and after surgery. FlowSight and FISH confirmed the CTCs detected by the telomerase-based method. To verify the correlation between CTCs and the immune response, peripheral white blood cell RNA sequencing was performed. Results CTCs were common in the peripheral blood of glioma patients and were not correlated with the pathological classification or grade of patients. The results showed that the presence of postoperative CTCs but not preoperative CTCs in glioma patients was a poor prognostic factor. The level of postoperative CTCs, which predicts a poor prognosis after surgery, may be associated with neutrophils. RNA sequencing suggested that postoperative CTCs were positively correlated with innate immune responses, especially the activation of neutrophils and the generation of neutrophil extracellular traps, but negatively correlated with the cytotoxic response. Conclusions Our results showed that telomerase-positive CTCs can predict a poor prognosis of patients with glioma. Our results also showed a correlation between CTCs and the immune macroenvironment, which provides a new perspective for the treatment of glioma.
format article
author Wen Zhang
Tiancheng Qin
Zhenrong Yang
Liyuan Yin
Changyun Zhao
Lin Feng
Song Lin
Binlei Liu
Shujun Cheng
Kaitai Zhang
author_facet Wen Zhang
Tiancheng Qin
Zhenrong Yang
Liyuan Yin
Changyun Zhao
Lin Feng
Song Lin
Binlei Liu
Shujun Cheng
Kaitai Zhang
author_sort Wen Zhang
title Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
title_short Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
title_full Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
title_fullStr Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
title_full_unstemmed Telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
title_sort telomerase-positive circulating tumor cells are associated with poor prognosis via a neutrophil-mediated inflammatory immune environment in glioma
publisher BMC
publishDate 2021
url https://doaj.org/article/3f9330ab146a4664a2e90a634a1500f3
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AT tianchengqin telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT zhenrongyang telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT liyuanyin telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT changyunzhao telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT linfeng telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT songlin telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT binleiliu telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT shujuncheng telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
AT kaitaizhang telomerasepositivecirculatingtumorcellsareassociatedwithpoorprognosisviaaneutrophilmediatedinflammatoryimmuneenvironmentinglioma
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