Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro

Lymphovascular invasion (LVI), encompassing blood and lymphatic vessel invasion, is an important event in tumourigenesis. Macrophages within the tumour microenvironment are linked to the presence of LVI and angiogenesis. This study investigates the role of macrophage-derived, caspase-1 dependent int...

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Main Authors: Storr, Sarah J., Safuan, Sabreena, Ahmad, Narmeen, El-Refaee, Mohammed, Jackson, Andrew M., Martin, Stewart G.
Format: Article
Published: Springer 2017
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Online Access:https://eprints.nottingham.ac.uk/43230/
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author Storr, Sarah J.
Safuan, Sabreena
Ahmad, Narmeen
El-Refaee, Mohammed
Jackson, Andrew M.
Martin, Stewart G.
author_facet Storr, Sarah J.
Safuan, Sabreena
Ahmad, Narmeen
El-Refaee, Mohammed
Jackson, Andrew M.
Martin, Stewart G.
author_sort Storr, Sarah J.
building Nottingham Research Data Repository
collection Online Access
description Lymphovascular invasion (LVI), encompassing blood and lymphatic vessel invasion, is an important event in tumourigenesis. Macrophages within the tumour microenvironment are linked to the presence of LVI and angiogenesis. This study investigates the role of macrophage-derived, caspase-1 dependent interleukin-1beta (IL-1β) in an in vitro model of LVI. IL-1β significantly augmented the adhesion and transmigration of breast cancer cell lines MCF7 and MDA-MB-231 across endothelial cell barriers. MDA-MB-231 and MCF7 showed a higher percentage of adhesion to lymphatic endothelial cells than blood endothelial cells following endothelial cell IL-1β stimulation (P<0.001 and P<0.0001 respectively). Supernatants from activated macrophages increased the adhesion of tumour cells to lymphatic and blood endothelium. Secretion of IL-1β was caspase-1 dependent, and treatment with caspase-1 inhibitor reduced IL-1β production by 73% and concomitantly reduced tumour cell adhesion to levels obtained with resting macrophages. Transmigration of MDA-MB-231 cells across blood and lymphatic endothelial monolayers was significantly increased following IL-1β stimulation. Furthermore, supernatants from activated macrophages increased transmigration of MDA-MB-231 cells across endothelial monolayers, which was abolished by caspase-1 inhibition. IL-1β stimulation of tumour cells significantly increased their migratory ability and a significant increase in migration was observed when MDA-MB-231 cells were stimulated with macrophage conditioned media (two of three donors). Results demonstrate that macrophage production of IL-1β plays an important role in the migration of breast cancer cells and their adhesion to, and transmigration across, blood and lymphatic endothelial cells. Results suggest that IL-1β may play a role in the adhesion to lymphatic endothelial cells in particular.
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spelling nottingham-432302024-08-15T15:22:40Z https://eprints.nottingham.ac.uk/43230/ Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro Storr, Sarah J. Safuan, Sabreena Ahmad, Narmeen El-Refaee, Mohammed Jackson, Andrew M. Martin, Stewart G. Lymphovascular invasion (LVI), encompassing blood and lymphatic vessel invasion, is an important event in tumourigenesis. Macrophages within the tumour microenvironment are linked to the presence of LVI and angiogenesis. This study investigates the role of macrophage-derived, caspase-1 dependent interleukin-1beta (IL-1β) in an in vitro model of LVI. IL-1β significantly augmented the adhesion and transmigration of breast cancer cell lines MCF7 and MDA-MB-231 across endothelial cell barriers. MDA-MB-231 and MCF7 showed a higher percentage of adhesion to lymphatic endothelial cells than blood endothelial cells following endothelial cell IL-1β stimulation (P<0.001 and P<0.0001 respectively). Supernatants from activated macrophages increased the adhesion of tumour cells to lymphatic and blood endothelium. Secretion of IL-1β was caspase-1 dependent, and treatment with caspase-1 inhibitor reduced IL-1β production by 73% and concomitantly reduced tumour cell adhesion to levels obtained with resting macrophages. Transmigration of MDA-MB-231 cells across blood and lymphatic endothelial monolayers was significantly increased following IL-1β stimulation. Furthermore, supernatants from activated macrophages increased transmigration of MDA-MB-231 cells across endothelial monolayers, which was abolished by caspase-1 inhibition. IL-1β stimulation of tumour cells significantly increased their migratory ability and a significant increase in migration was observed when MDA-MB-231 cells were stimulated with macrophage conditioned media (two of three donors). Results demonstrate that macrophage production of IL-1β plays an important role in the migration of breast cancer cells and their adhesion to, and transmigration across, blood and lymphatic endothelial cells. Results suggest that IL-1β may play a role in the adhesion to lymphatic endothelial cells in particular. Springer 2017-05-27 Article PeerReviewed Storr, Sarah J., Safuan, Sabreena, Ahmad, Narmeen, El-Refaee, Mohammed, Jackson, Andrew M. and Martin, Stewart G. (2017) Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro. Cancer Immunology, Immunotherapy . ISSN 0340-7004 interleukin-1; breast cancer; macrophage; vascular invasion; caspase-1 https://link.springer.com/article/10.1007%2Fs00262-017-2020-0 doi:10.1007/s00262-017-2020-0 doi:10.1007/s00262-017-2020-0
spellingShingle interleukin-1; breast cancer; macrophage; vascular invasion; caspase-1
Storr, Sarah J.
Safuan, Sabreena
Ahmad, Narmeen
El-Refaee, Mohammed
Jackson, Andrew M.
Martin, Stewart G.
Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
title Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
title_full Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
title_fullStr Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
title_full_unstemmed Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
title_short Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
title_sort macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro
topic interleukin-1; breast cancer; macrophage; vascular invasion; caspase-1
url https://eprints.nottingham.ac.uk/43230/
https://eprints.nottingham.ac.uk/43230/
https://eprints.nottingham.ac.uk/43230/