Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells

Wen Zhang; Li Bao; Shaoxing Yang; Zhaoyang Qian; Mei Dong; Liyuan Yin; Qian Zhao; Keli Ge; Zhenling Deng; Jing Zhang; Fei Qi; Zhongxue An; Yuan Yu; Qingbo Wang; Renhua Wu; Fan Fan; Lianfeng Zhang; Xiping Chen; Yingjian Na; Lin Feng; Lingling Liu; Yujie Zhu; Tiancheng Qin; Shuren Zhang; Youhui Zhang; Xiuqing Zhang; Jian Wang; Xin Yi; Liqun Zou; Hong-Wu Xin; Henrik J Ditzel; Hongjun Gao; Kaitai Zhang; Binlei Liu; Shujun Cheng

doi:10.18632/oncotarget.9465

Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells

Wen Zhang, Li Bao, Shaoxing Yang, Zhaoyang Qian, Mei Dong, Liyuan Yin, Qian Zhao, Keli Ge, Zhenling Deng, Jing Zhang, Fei Qi, Zhongxue An, Yuan Yu, Qingbo Wang, Renhua Wu, Fan Fan, Lianfeng Zhang, Xiping Chen, Yingjian Na, Lin FengLingling Liu, Yujie Zhu, Tiancheng Qin, Shuren Zhang, Youhui Zhang, Xiuqing Zhang, Jian Wang, Xin Yi, Liqun Zou, Hong-Wu Xin, Henrik J Ditzel, Hongjun Gao, Kaitai Zhang, Binlei Liu, Shujun Cheng

21 Citationer (Scopus)

Abstract

Detection of circulating tumor cells remains a significant challenge due to their vast physical and biological heterogeneity. We developed a cell-surface-marker-independent technology based on telomerase-specific, replication-selective oncolytic herpes-simplex-virus-1 that targets telomerase-reverse-transcriptase-positive cancer cells and expresses green-fluorescent-protein that identifies viable CTCs from a broad spectrum of malignancies. Our method recovered 75.5-87.2% of tumor cells spiked into healthy donor blood, as validated by different methods, including single cell sequencing. CTCs were detected in 59-100% of 326 blood samples from patients with 6 different solid organ carcinomas and lymphomas. Significantly, CTC-positive rates increased remarkably with tumor progression from N0M0, N+M0 to M1 in each of 5 tested cancers (lung, colon, liver, gastric and pancreatic cancer, and glioma). Among 21 non-small cell lung cancer cases in which CTC values were consecutively monitored, 81% showed treatment-related decreases, which was also found after treatments in the other solid tumors. Moreover, monitoring CTC values provided an efficient treatment response indicator in hematological malignancies. Compared to CellSearch, our method detected significantly higher positive rates in 40 NSCLC in all stages, including N0M0, N+M0 and M1, and was less affected by chemotherapy. This simple, robust and clinically-applicable technology detects viable CTCs from solid and hematopoietic malignancies in early to late stages, and significantly improves clinical detection and treatment prognostication.

Originalsprog	Engelsk
Tidsskrift	OncoTarget
Vol/bind	7
Udgave nummer	26
Sider (fra-til)	39768-39783
ISSN	1949-2553
DOI	https://doi.org/10.18632/oncotarget.9465
Status	Udgivet - 18 maj 2016

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10.18632/oncotarget.9465Licens: CC BY

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Zhang, W., Bao, L., Yang, S., Qian, Z., Dong, M., Yin, L., Zhao, Q., Ge, K., Deng, Z., Zhang, J., Qi, F., An, Z., Yu, Y., Wang, Q., Wu, R., Fan, F., Zhang, L., Chen, X., Na, Y., ... Cheng, S. (2016). Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells. OncoTarget, 7(26), 39768-39783. https://doi.org/10.18632/oncotarget.9465

Zhang, W, Bao, L, Yang, S, Qian, Z, Dong, M, Yin, L, Zhao, Q, Ge, K, Deng, Z, Zhang, J, Qi, F, An, Z, Yu, Y, Wang, Q, Wu, R, Fan, F, Zhang, L, Chen, X, Na, Y, Feng, L, Liu, L, Zhu, Y, Qin, T, Zhang, S, Zhang, Y, Zhang, X, Wang, J, Yi, X, Zou, L, Xin, H-W, Ditzel, HJ, Gao, H, Zhang, K, Liu, B & Cheng, S 2016, 'Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells', OncoTarget, bind 7, nr. 26, s. 39768-39783. https://doi.org/10.18632/oncotarget.9465

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title = "Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells",

abstract = "Detection of circulating tumor cells remains a significant challenge due to their vast physical and biological heterogeneity. We developed a cell-surface-marker-independent technology based on telomerase-specific, replication-selective oncolytic herpes-simplex-virus-1 that targets telomerase-reverse-transcriptase-positive cancer cells and expresses green-fluorescent-protein that identifies viable CTCs from a broad spectrum of malignancies. Our method recovered 75.5-87.2% of tumor cells spiked into healthy donor blood, as validated by different methods, including single cell sequencing. CTCs were detected in 59-100% of 326 blood samples from patients with 6 different solid organ carcinomas and lymphomas. Significantly, CTC-positive rates increased remarkably with tumor progression from N0M0, N+M0 to M1 in each of 5 tested cancers (lung, colon, liver, gastric and pancreatic cancer, and glioma). Among 21 non-small cell lung cancer cases in which CTC values were consecutively monitored, 81% showed treatment-related decreases, which was also found after treatments in the other solid tumors. Moreover, monitoring CTC values provided an efficient treatment response indicator in hematological malignancies. Compared to CellSearch, our method detected significantly higher positive rates in 40 NSCLC in all stages, including N0M0, N+M0 and M1, and was less affected by chemotherapy. This simple, robust and clinically-applicable technology detects viable CTCs from solid and hematopoietic malignancies in early to late stages, and significantly improves clinical detection and treatment prognostication.",

author = "Wen Zhang and Li Bao and Shaoxing Yang and Zhaoyang Qian and Mei Dong and Liyuan Yin and Qian Zhao and Keli Ge and Zhenling Deng and Jing Zhang and Fei Qi and Zhongxue An and Yuan Yu and Qingbo Wang and Renhua Wu and Fan Fan and Lianfeng Zhang and Xiping Chen and Yingjian Na and Lin Feng and Lingling Liu and Yujie Zhu and Tiancheng Qin and Shuren Zhang and Youhui Zhang and Xiuqing Zhang and Jian Wang and Xin Yi and Liqun Zou and Hong-Wu Xin and Ditzel, {Henrik J} and Hongjun Gao and Kaitai Zhang and Binlei Liu and Shujun Cheng",

year = "2016",

month = may,

day = "18",

doi = "10.18632/oncotarget.9465",

language = "English",

volume = "7",

pages = "39768--39783",

journal = "OncoTarget",

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TY - JOUR

T1 - Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells

AU - Zhang, Wen

AU - Bao, Li

AU - Yang, Shaoxing

AU - Qian, Zhaoyang

AU - Dong, Mei

AU - Yin, Liyuan

AU - Zhao, Qian

AU - Ge, Keli

AU - Deng, Zhenling

AU - Zhang, Jing

AU - Qi, Fei

AU - An, Zhongxue

AU - Yu, Yuan

AU - Wang, Qingbo

AU - Wu, Renhua

AU - Fan, Fan

AU - Zhang, Lianfeng

AU - Chen, Xiping

AU - Na, Yingjian

AU - Feng, Lin

AU - Liu, Lingling

AU - Zhu, Yujie

AU - Qin, Tiancheng

AU - Zhang, Shuren

AU - Zhang, Youhui

AU - Zhang, Xiuqing

AU - Wang, Jian

AU - Yi, Xin

AU - Zou, Liqun

AU - Xin, Hong-Wu

AU - Ditzel, Henrik J

AU - Gao, Hongjun

AU - Zhang, Kaitai

AU - Liu, Binlei

AU - Cheng, Shujun

PY - 2016/5/18

Y1 - 2016/5/18

N2 - Detection of circulating tumor cells remains a significant challenge due to their vast physical and biological heterogeneity. We developed a cell-surface-marker-independent technology based on telomerase-specific, replication-selective oncolytic herpes-simplex-virus-1 that targets telomerase-reverse-transcriptase-positive cancer cells and expresses green-fluorescent-protein that identifies viable CTCs from a broad spectrum of malignancies. Our method recovered 75.5-87.2% of tumor cells spiked into healthy donor blood, as validated by different methods, including single cell sequencing. CTCs were detected in 59-100% of 326 blood samples from patients with 6 different solid organ carcinomas and lymphomas. Significantly, CTC-positive rates increased remarkably with tumor progression from N0M0, N+M0 to M1 in each of 5 tested cancers (lung, colon, liver, gastric and pancreatic cancer, and glioma). Among 21 non-small cell lung cancer cases in which CTC values were consecutively monitored, 81% showed treatment-related decreases, which was also found after treatments in the other solid tumors. Moreover, monitoring CTC values provided an efficient treatment response indicator in hematological malignancies. Compared to CellSearch, our method detected significantly higher positive rates in 40 NSCLC in all stages, including N0M0, N+M0 and M1, and was less affected by chemotherapy. This simple, robust and clinically-applicable technology detects viable CTCs from solid and hematopoietic malignancies in early to late stages, and significantly improves clinical detection and treatment prognostication.

AB - Detection of circulating tumor cells remains a significant challenge due to their vast physical and biological heterogeneity. We developed a cell-surface-marker-independent technology based on telomerase-specific, replication-selective oncolytic herpes-simplex-virus-1 that targets telomerase-reverse-transcriptase-positive cancer cells and expresses green-fluorescent-protein that identifies viable CTCs from a broad spectrum of malignancies. Our method recovered 75.5-87.2% of tumor cells spiked into healthy donor blood, as validated by different methods, including single cell sequencing. CTCs were detected in 59-100% of 326 blood samples from patients with 6 different solid organ carcinomas and lymphomas. Significantly, CTC-positive rates increased remarkably with tumor progression from N0M0, N+M0 to M1 in each of 5 tested cancers (lung, colon, liver, gastric and pancreatic cancer, and glioma). Among 21 non-small cell lung cancer cases in which CTC values were consecutively monitored, 81% showed treatment-related decreases, which was also found after treatments in the other solid tumors. Moreover, monitoring CTC values provided an efficient treatment response indicator in hematological malignancies. Compared to CellSearch, our method detected significantly higher positive rates in 40 NSCLC in all stages, including N0M0, N+M0 and M1, and was less affected by chemotherapy. This simple, robust and clinically-applicable technology detects viable CTCs from solid and hematopoietic malignancies in early to late stages, and significantly improves clinical detection and treatment prognostication.

U2 - 10.18632/oncotarget.9465

DO - 10.18632/oncotarget.9465

M3 - Journal article

C2 - 27206795

SN - 1949-2553

VL - 7

SP - 39768

EP - 39783

JO - OncoTarget

JF - OncoTarget

IS - 26

ER -

Tumor-selective replication herpes simplex virus-based technology significantly improves clinical detection and prognostication of viable circulating tumor cells

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