Morphological quantification of proliferation-to-invasion transition in tumor spheroids

Yi He, Ling Xiong, Xuejuan Gao, Miaomiao Hai, Yanping Liu, Gao Wang, Guo Chen, Jianwei Shuai, Yang Jiao, Xixiang Zhang, Ruchuan Liu, Liyu Liu

Research output: Contribution to journalArticle

Abstract

Background: Metastasis determines the lethality of cancer. In most clinical cases, patients are able to live with tumor proliferation before metastasis. Thus, the transition from tumor proliferation to metastasis/invasion is essential. However, the mechanism is still unclear and especially, the proliferation-to-metastasis/invasion transition point has not been well defined. Therefore, quantitative characterization of this transition is urgently needed. Methods: We have successfully developed a home-built living-cell incubation system combined with an inverted optical microscope, and a systematic, quantitative approach to describing the major characteristic morphological parameters for the identification of the critical transition points for tumor-cell spheroids in a collagen fiber scaffold. Results: The system focuses on in vitro tumor modeling, e.g. the development of tumor-cell spheroids in a collagen fiber scaffold and the monitoring of cell transition from proliferation to invasion. By applying this approach to multiple tumor spheroid models, such as U87 (glioma tumor), H1299 (lung cancer), and MDA-MB-231 (breast cancer) cells, we have obtained quantitative morphological references to evaluate the proliferation-to-invasion transition time, as well as differentiating the invasion potential of tumor cells upon environmental changes, i.e. drug application. Conclusions: Our quantitative approach provides a feasible clarification for the proliferation-to-invasion transition of in vitro tumor models (spheroids). Moreover, the transition time is a useful reference for the invasive potential of tumor cells. General significance: This quantitative approach is potentially applicable to primary tumor cells, and thus has potential applications in the fields of cancer metastasis investigations and clinical diagnostics.

Original languageEnglish (US)
Article number129460
JournalBiochimica et Biophysica Acta - General Subjects
Volume1864
Issue number1
DOIs
StatePublished - Jan 2020

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Tumors
Neoplasms
Neoplasm Metastasis
Cells
Scaffolds
Collagen
Fibers
Glioma
Microscopes
Lung Neoplasms
Cell Proliferation
Breast Neoplasms
Monitoring
Pharmaceutical Preparations

Keywords

  • Cancer invasion
  • Image processing
  • Living-cell device
  • Quantitative analysis
  • Transition time
  • Tumor spheroids model

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Molecular Biology

Cite this

Morphological quantification of proliferation-to-invasion transition in tumor spheroids. / He, Yi; Xiong, Ling; Gao, Xuejuan; Hai, Miaomiao; Liu, Yanping; Wang, Gao; Chen, Guo; Shuai, Jianwei; Jiao, Yang; Zhang, Xixiang; Liu, Ruchuan; Liu, Liyu.

In: Biochimica et Biophysica Acta - General Subjects, Vol. 1864, No. 1, 129460, 01.2020.

Research output: Contribution to journalArticle

He, Y, Xiong, L, Gao, X, Hai, M, Liu, Y, Wang, G, Chen, G, Shuai, J, Jiao, Y, Zhang, X, Liu, R & Liu, L 2020, 'Morphological quantification of proliferation-to-invasion transition in tumor spheroids', Biochimica et Biophysica Acta - General Subjects, vol. 1864, no. 1, 129460. https://doi.org/10.1016/j.bbagen.2019.129460
He, Yi ; Xiong, Ling ; Gao, Xuejuan ; Hai, Miaomiao ; Liu, Yanping ; Wang, Gao ; Chen, Guo ; Shuai, Jianwei ; Jiao, Yang ; Zhang, Xixiang ; Liu, Ruchuan ; Liu, Liyu. / Morphological quantification of proliferation-to-invasion transition in tumor spheroids. In: Biochimica et Biophysica Acta - General Subjects. 2020 ; Vol. 1864, No. 1.
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abstract = "Background: Metastasis determines the lethality of cancer. In most clinical cases, patients are able to live with tumor proliferation before metastasis. Thus, the transition from tumor proliferation to metastasis/invasion is essential. However, the mechanism is still unclear and especially, the proliferation-to-metastasis/invasion transition point has not been well defined. Therefore, quantitative characterization of this transition is urgently needed. Methods: We have successfully developed a home-built living-cell incubation system combined with an inverted optical microscope, and a systematic, quantitative approach to describing the major characteristic morphological parameters for the identification of the critical transition points for tumor-cell spheroids in a collagen fiber scaffold. Results: The system focuses on in vitro tumor modeling, e.g. the development of tumor-cell spheroids in a collagen fiber scaffold and the monitoring of cell transition from proliferation to invasion. By applying this approach to multiple tumor spheroid models, such as U87 (glioma tumor), H1299 (lung cancer), and MDA-MB-231 (breast cancer) cells, we have obtained quantitative morphological references to evaluate the proliferation-to-invasion transition time, as well as differentiating the invasion potential of tumor cells upon environmental changes, i.e. drug application. Conclusions: Our quantitative approach provides a feasible clarification for the proliferation-to-invasion transition of in vitro tumor models (spheroids). Moreover, the transition time is a useful reference for the invasive potential of tumor cells. General significance: This quantitative approach is potentially applicable to primary tumor cells, and thus has potential applications in the fields of cancer metastasis investigations and clinical diagnostics.",
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T1 - Morphological quantification of proliferation-to-invasion transition in tumor spheroids

AU - He, Yi

AU - Xiong, Ling

AU - Gao, Xuejuan

AU - Hai, Miaomiao

AU - Liu, Yanping

AU - Wang, Gao

AU - Chen, Guo

AU - Shuai, Jianwei

AU - Jiao, Yang

AU - Zhang, Xixiang

AU - Liu, Ruchuan

AU - Liu, Liyu

PY - 2020/1

Y1 - 2020/1

N2 - Background: Metastasis determines the lethality of cancer. In most clinical cases, patients are able to live with tumor proliferation before metastasis. Thus, the transition from tumor proliferation to metastasis/invasion is essential. However, the mechanism is still unclear and especially, the proliferation-to-metastasis/invasion transition point has not been well defined. Therefore, quantitative characterization of this transition is urgently needed. Methods: We have successfully developed a home-built living-cell incubation system combined with an inverted optical microscope, and a systematic, quantitative approach to describing the major characteristic morphological parameters for the identification of the critical transition points for tumor-cell spheroids in a collagen fiber scaffold. Results: The system focuses on in vitro tumor modeling, e.g. the development of tumor-cell spheroids in a collagen fiber scaffold and the monitoring of cell transition from proliferation to invasion. By applying this approach to multiple tumor spheroid models, such as U87 (glioma tumor), H1299 (lung cancer), and MDA-MB-231 (breast cancer) cells, we have obtained quantitative morphological references to evaluate the proliferation-to-invasion transition time, as well as differentiating the invasion potential of tumor cells upon environmental changes, i.e. drug application. Conclusions: Our quantitative approach provides a feasible clarification for the proliferation-to-invasion transition of in vitro tumor models (spheroids). Moreover, the transition time is a useful reference for the invasive potential of tumor cells. General significance: This quantitative approach is potentially applicable to primary tumor cells, and thus has potential applications in the fields of cancer metastasis investigations and clinical diagnostics.

AB - Background: Metastasis determines the lethality of cancer. In most clinical cases, patients are able to live with tumor proliferation before metastasis. Thus, the transition from tumor proliferation to metastasis/invasion is essential. However, the mechanism is still unclear and especially, the proliferation-to-metastasis/invasion transition point has not been well defined. Therefore, quantitative characterization of this transition is urgently needed. Methods: We have successfully developed a home-built living-cell incubation system combined with an inverted optical microscope, and a systematic, quantitative approach to describing the major characteristic morphological parameters for the identification of the critical transition points for tumor-cell spheroids in a collagen fiber scaffold. Results: The system focuses on in vitro tumor modeling, e.g. the development of tumor-cell spheroids in a collagen fiber scaffold and the monitoring of cell transition from proliferation to invasion. By applying this approach to multiple tumor spheroid models, such as U87 (glioma tumor), H1299 (lung cancer), and MDA-MB-231 (breast cancer) cells, we have obtained quantitative morphological references to evaluate the proliferation-to-invasion transition time, as well as differentiating the invasion potential of tumor cells upon environmental changes, i.e. drug application. Conclusions: Our quantitative approach provides a feasible clarification for the proliferation-to-invasion transition of in vitro tumor models (spheroids). Moreover, the transition time is a useful reference for the invasive potential of tumor cells. General significance: This quantitative approach is potentially applicable to primary tumor cells, and thus has potential applications in the fields of cancer metastasis investigations and clinical diagnostics.

KW - Cancer invasion

KW - Image processing

KW - Living-cell device

KW - Quantitative analysis

KW - Transition time

KW - Tumor spheroids model

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