Role of neutrophil extracellular traps in regulation of lung cancer invasion and metastasis: Structural insights from a computational model
Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive metastasis. Neutrophils, which in their original form should establish immune activities to the tumor as a first line of defense, are undermine...
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| Published in | PLoS computational biology Vol. 17; no. 2; p. e1008257 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2021
Public Library of Science (PLoS) |
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| Online Access | Get full text |
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| Abstract | Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive metastasis. Neutrophils, which in their original form should establish immune activities to the tumor as a first line of defense, are undermined by tumor cells to promote tumor invasion in several ways. In this study, we investigate the mutual interactions between the tumor cells and the neutrophils that facilitate tumor invasion by developing a mathematical model that involves taxis-reaction-diffusion equations for the critical components in the interaction. These include the densities of tumor and neutrophils, and the concentrations of signaling molecules and structure such as neutrophil extracellular traps (NETs). We apply the mathematical model to a Boyden invasion assay used in the experiments to demonstrate that the tumor-associated neutrophils can enhance tumor cell invasion by secreting the neutrophil elastase. We show that the model can both reproduce the major experimental observation on NET-mediated cancer invasion and make several important predictions to guide future experiments with the goal of the development of new anti-tumor strategies. Moreover, using this model, we investigate the fundamental mechanism of NET-mediated invasion of cancer cells and the impact of internal and external heterogeneity on the migration patterning of tumour cells and their response to different treatment schedules. |
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| AbstractList | Tumor-associated neutrophils (TANs) are of particular interest because experimental studies showed that they can contribute to the tumor growth, critical invasion, epithelial-mesenchymal transition (EMT), and metastasis of cancer cells [3, 4]. [...]recently, neutrophils have been considered as merely a bystander in the TME and metastasis [5–7] but they are emerging as an important player due to consistent and continuous evidences of their tumor-promoting roles [3]. In homeostasis of normal tissue, these pathways are balanced so as to control growth, but in lung cancer, increased secretion of TGF-β by tumor cells induces the N1→N2 transition of the neutrophils and stimulates their secretion of NE and other growth factors. An extracellular matrix (ECM) layer (S) surrounds the filter, semi-permeable membrane (). https://doi.org/10.1371/journal.pcbi.1008257.g002 Materials and methods We developed a mathematical model of tumor cell invasion in in vitro experiments, a critical step in metastasis [22, 47, 48], based on mutual interactions between tumor cells and neutrophils (Fig 1). The net production of tumor cells is due to active NE-stimulated growth [8, 22] and cell killing by N1 TANs [3, 21, 23], which we represent as follows:(5)Here r is the proliferation rate of tumor cells in the absence of NE (E), rE is the dimensionless parameter of NE-mediated tumor growth, kE and m are Hill-function coefficients for activation of proliferation in the presence of NE, n0 is the carrying capacity of the tumor in a given TME, and, finally μn is the killing rate of tumor cells by N1 neutrophils (N1) whose dynamics will be described in Section ‘Densities of neutrophils’ below. Tumor-associated neutrophils (TANs) are of particular interest because experimental studies showed that they can contribute to the tumor growth, critical invasion, epithelial-mesenchymal transition (EMT), and metastasis of cancer cells [3, 4]. [...]recently, neutrophils have been considered as merely a bystander in the TME and metastasis [5–7] but they are emerging as an important player due to consistent and continuous evidences of their tumor-promoting roles [3]. In homeostasis of normal tissue, these pathways are balanced so as to control growth, but in lung cancer, increased secretion of TGF-β by tumor cells induces the N1→N2 transition of the neutrophils and stimulates their secretion of NE and other growth factors. An extracellular matrix (ECM) layer (S) surrounds the filter, semi-permeable membrane (). https://doi.org/10.1371/journal.pcbi.1008257.g002 Materials and methods We developed a mathematical model of tumor cell invasion in in vitro experiments, a critical step in metastasis [22, 47, 48], based on mutual interactions between tumor cells and neutrophils (Fig 1). The net production of tumor cells is due to active NE-stimulated growth [8, 22] and cell killing by N1 TANs [3, 21, 23], which we represent as follows:(5)Here r is the proliferation rate of tumor cells in the absence of NE (E), rE is the dimensionless parameter of NE-mediated tumor growth, kE and m are Hill-function coefficients for activation of proliferation in the presence of NE, n0 is the carrying capacity of the tumor in a given TME, and, finally μn is the killing rate of tumor cells by N1 neutrophils (N1) whose dynamics will be described in Section ‘Densities of neutrophils’ below. Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive metastasis. Neutrophils, which in their original form should establish immune activities to the tumor as a first line of defense, are undermined by tumor cells to promote tumor invasion in several ways. In this study, we investigate the mutual interactions between the tumor cells and the neutrophils that facilitate tumor invasion by developing a mathematical model that involves taxis-reaction-diffusion equations for the critical components in the interaction. These include the densities of tumor and neutrophils, and the concentrations of signaling molecules and structure such as neutrophil extracellular traps (NETs). We apply the mathematical model to a Boyden invasion assay used in the experiments to demonstrate that the tumor-associated neutrophils can enhance tumor cell invasion by secreting the neutrophil elastase. We show that the model can both reproduce the major experimental observation on NET-mediated cancer invasion and make several important predictions to guide future experiments with the goal of the development of new anti-tumor strategies. Moreover, using this model, we investigate the fundamental mechanism of NET-mediated invasion of cancer cells and the impact of internal and external heterogeneity on the migration patterning of tumour cells and their response to different treatment schedules.Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive metastasis. Neutrophils, which in their original form should establish immune activities to the tumor as a first line of defense, are undermined by tumor cells to promote tumor invasion in several ways. In this study, we investigate the mutual interactions between the tumor cells and the neutrophils that facilitate tumor invasion by developing a mathematical model that involves taxis-reaction-diffusion equations for the critical components in the interaction. These include the densities of tumor and neutrophils, and the concentrations of signaling molecules and structure such as neutrophil extracellular traps (NETs). We apply the mathematical model to a Boyden invasion assay used in the experiments to demonstrate that the tumor-associated neutrophils can enhance tumor cell invasion by secreting the neutrophil elastase. We show that the model can both reproduce the major experimental observation on NET-mediated cancer invasion and make several important predictions to guide future experiments with the goal of the development of new anti-tumor strategies. Moreover, using this model, we investigate the fundamental mechanism of NET-mediated invasion of cancer cells and the impact of internal and external heterogeneity on the migration patterning of tumour cells and their response to different treatment schedules. Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive metastasis. Neutrophils, which in their original form should establish immune activities to the tumor as a first line of defense, are undermined by tumor cells to promote tumor invasion in several ways. In this study, we investigate the mutual interactions between the tumor cells and the neutrophils that facilitate tumor invasion by developing a mathematical model that involves taxis-reaction-diffusion equations for the critical components in the interaction. These include the densities of tumor and neutrophils, and the concentrations of signaling molecules and structure such as neutrophil extracellular traps (NETs). We apply the mathematical model to a Boyden invasion assay used in the experiments to demonstrate that the tumor-associated neutrophils can enhance tumor cell invasion by secreting the neutrophil elastase. We show that the model can both reproduce the major experimental observation on NET-mediated cancer invasion and make several important predictions to guide future experiments with the goal of the development of new anti-tumor strategies. Moreover, using this model, we investigate the fundamental mechanism of NET-mediated invasion of cancer cells and the impact of internal and external heterogeneity on the migration patterning of tumour cells and their response to different treatment schedules. Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive metastasis. Neutrophils, which in their original form should establish immune activities to the tumor as a first line of defense, are undermined by tumor cells to promote tumor invasion in several ways. In this study, we investigate the mutual interactions between the tumor cells and the neutrophils that facilitate tumor invasion by developing a mathematical model that involves taxis-reaction-diffusion equations for the critical components in the interaction. These include the densities of tumor and neutrophils, and the concentrations of signaling molecules and structure such as neutrophil extracellular traps (NETs). We apply the mathematical model to a Boyden invasion assay used in the experiments to demonstrate that the tumor-associated neutrophils can enhance tumor cell invasion by secreting the neutrophil elastase. We show that the model can both reproduce the major experimental observation on NET-mediated cancer invasion and make several important predictions to guide future experiments with the goal of the development of new anti-tumor strategies. Moreover, using this model, we investigate the fundamental mechanism of NET-mediated invasion of cancer cells and the impact of internal and external heterogeneity on the migration patterning of tumour cells and their response to different treatment schedules. When cancer patients are diagnosed with tumours at a primary site, the cancer cells are often found in the blood or already metastasized to the secondary sites in other organs. These metastatic cancer cells are more resistant to major anti-cancer therapies, and lead to the low survival probability. Until recently, the role of neutrophils, specifically tumor-associated neutrophils as a member of complex tumor microenvironment, has been ignored for a long time due to technical difficulties in tumor biology but these neutrophils are emerging as an important player in regulation of tumor invasion and metastasis. The mutual interaction between a tumor and neutrophils from bone marrow or in blood induces the critical transition of the naive form, called the N1 type, to the more aggressive phenotype, called the N2 TANs, which then promotes tumor invasion. In this article, we investigate how stimulated neutrophils with different N1 and N2 landscapes shape the metastatic potential of the lung cancers. Our simulation framework is designed for boyden invasion chamber in experiments and based on a mathematical model that describes how tumor cells interact with neutrophils and N2 TANs can promote tumor cell invasion. We demonstrate that the efficacy of anti-tumor (anti-invasion) drugs depend on this critical communication and N1→N2 landscapes of stimulated neutrophils. |
| Author | Lee, Junho Lee, Donggu Lawler, Sean Kim, Yangjin |
| AuthorAffiliation | University of Southern California, UNITED STATES 1 Department of Mathematics, Konkuk University, Seoul, Republic of Korea 2 Mathematical Biosciences Institute, Ohio State University, Columbus, Ohio, United States of America 3 Department of neurosurgery, Brigham and Women’s Hospital & Harvard Medical School, Boston, Massachusetts, United States of America |
| AuthorAffiliation_xml | – name: 2 Mathematical Biosciences Institute, Ohio State University, Columbus, Ohio, United States of America – name: University of Southern California, UNITED STATES – name: 3 Department of neurosurgery, Brigham and Women’s Hospital & Harvard Medical School, Boston, Massachusetts, United States of America – name: 1 Department of Mathematics, Konkuk University, Seoul, Republic of Korea |
| Author_xml | – sequence: 1 givenname: Junho orcidid: 0000-0003-4342-5693 surname: Lee fullname: Lee, Junho – sequence: 2 givenname: Donggu orcidid: 0000-0001-7642-5601 surname: Lee fullname: Lee, Donggu – sequence: 3 givenname: Sean surname: Lawler fullname: Lawler, Sean – sequence: 4 givenname: Yangjin orcidid: 0000-0002-8905-8481 surname: Kim fullname: Kim, Yangjin |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33596197$$D View this record in MEDLINE/PubMed |
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| Copyright | 2021 Lee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 Lee et al 2021 Lee et al |
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| DOI | 10.1371/journal.pcbi.1008257 |
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| Snippet | Lung cancer is one of the leading causes of cancer-related deaths worldwide and is characterized by hijacking immune system for active growth and aggressive... Tumor-associated neutrophils (TANs) are of particular interest because experimental studies showed that they can contribute to the tumor growth, critical... |
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| SubjectTerms | Biology and Life Sciences Carrying capacity Cell proliferation Chemokines Clinical outcomes Computational Biology Computer applications Computer Simulation Extracellular matrix Extracellular Traps - metabolism Fibroblasts Growth factors Homeostasis Humans In Vitro Techniques Interleukin-8 - antagonists & inhibitors Leukocytes (neutrophilic) Lung cancer Lung Neoplasms - metabolism Lung Neoplasms - pathology Lung Neoplasms - therapy Mathematical models Matrix methods Medicine and Health Sciences Mesenchyme Metastases Metastasis Models, Biological Motility Neoplasm Invasiveness - pathology Neoplasm Metastasis - pathology Neutrophils Neutrophils - metabolism Neutrophils - pathology Receptors, Transforming Growth Factor beta - antagonists & inhibitors Research and Analysis Methods Secretion Signal Transduction Transforming Growth Factor beta - antagonists & inhibitors Tumor cells Tumor Microenvironment Tumors |
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| Title | Role of neutrophil extracellular traps in regulation of lung cancer invasion and metastasis: Structural insights from a computational model |
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