Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression

Summary: Transforming growth factor β (TGF-β) is abundantly present in the tumor microenvironment, contributing to cancer progression. However, the regulatory mechanism by which TGF-β affects vascular endothelial cells (ECs) in the tumor microenvironment is not well understood. Herein, we generated...

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Main Authors: Kako Hanada, Yuki Saito, Takahiro Takagi, Mitsuki Go, Yota Nakano, Toshihiko Inagawa, Hideyo Hirai, Marcus Fruttiger, Susumu Itoh, Fumiko Itoh
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004224027299
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author Kako Hanada
Yuki Saito
Takahiro Takagi
Mitsuki Go
Yota Nakano
Toshihiko Inagawa
Hideyo Hirai
Marcus Fruttiger
Susumu Itoh
Fumiko Itoh
author_facet Kako Hanada
Yuki Saito
Takahiro Takagi
Mitsuki Go
Yota Nakano
Toshihiko Inagawa
Hideyo Hirai
Marcus Fruttiger
Susumu Itoh
Fumiko Itoh
author_sort Kako Hanada
collection DOAJ
description Summary: Transforming growth factor β (TGF-β) is abundantly present in the tumor microenvironment, contributing to cancer progression. However, the regulatory mechanism by which TGF-β affects vascular endothelial cells (ECs) in the tumor microenvironment is not well understood. Herein, we generated tamoxifen-inducible TGF-β type II receptor (TβRII) knockout mice, specifically targeting ECs (TβRIIiΔEC), by crossbreeding TβRII-floxed mice with Pdgfb-icreER mice. We established tumor-bearing mice by transplanting Lewis lung carcinoma (LLC) cells. TβRIIiΔEC mice exhibited increased tumor angiogenesis with fragile new blood vessels, increased bleeding, and hypoxia compared to control mice. Consequently, the compromised tumor microenvironment precipitated a notable surge in circulating tumor cells. Paradoxically, lung metastasis showed a significant decline. This intriguing discrepancy was explained by a reduction in the engraftment between cancer cells and ECs. Disruption of TGF-β signaling downregulated CD44 on ECs, hindering cancer cell adhesion. These findings highlight TGF-β′s role in promoting metastasis by modulating EC function.
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spelling doaj-art-57eb9d904df841ccacef2b86e665470a2025-08-20T02:39:38ZengElsevieriScience2589-00422024-12-01271211150210.1016/j.isci.2024.111502Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expressionKako Hanada0Yuki Saito1Takahiro Takagi2Mitsuki Go3Yota Nakano4Toshihiko Inagawa5Hideyo Hirai6Marcus Fruttiger7Susumu Itoh8Fumiko Itoh9Laboratory of Stem Cell Regulation, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, Japan; Laboratory of Cardiovascular Medicine, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanLaboratory of Cardiovascular Medicine, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanLaboratory of Cardiovascular Medicine, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanLaboratory of Cardiovascular Medicine, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanLaboratory of Biochemistry, Showa Pharmaceutical University, 3-3165 Higashi-Tamagawagakuen, Machida, Tokyo 194-8543, JapanLaboratory of Cardiovascular Medicine, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanLaboratory of Stem Cell Regulation, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanUCL Institute of Ophthalmology, University College London, 11-43 Bath Street, London EC1V 9EL, UKLaboratory of Biochemistry, Showa Pharmaceutical University, 3-3165 Higashi-Tamagawagakuen, Machida, Tokyo 194-8543, JapanLaboratory of Stem Cell Regulation, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, Japan; Laboratory of Cardiovascular Medicine, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, Japan; Corresponding authorSummary: Transforming growth factor β (TGF-β) is abundantly present in the tumor microenvironment, contributing to cancer progression. However, the regulatory mechanism by which TGF-β affects vascular endothelial cells (ECs) in the tumor microenvironment is not well understood. Herein, we generated tamoxifen-inducible TGF-β type II receptor (TβRII) knockout mice, specifically targeting ECs (TβRIIiΔEC), by crossbreeding TβRII-floxed mice with Pdgfb-icreER mice. We established tumor-bearing mice by transplanting Lewis lung carcinoma (LLC) cells. TβRIIiΔEC mice exhibited increased tumor angiogenesis with fragile new blood vessels, increased bleeding, and hypoxia compared to control mice. Consequently, the compromised tumor microenvironment precipitated a notable surge in circulating tumor cells. Paradoxically, lung metastasis showed a significant decline. This intriguing discrepancy was explained by a reduction in the engraftment between cancer cells and ECs. Disruption of TGF-β signaling downregulated CD44 on ECs, hindering cancer cell adhesion. These findings highlight TGF-β′s role in promoting metastasis by modulating EC function.http://www.sciencedirect.com/science/article/pii/S2589004224027299Natural sciencesBiological sciencesSystems biologyCancer systems biologyCancer
spellingShingle Kako Hanada
Yuki Saito
Takahiro Takagi
Mitsuki Go
Yota Nakano
Toshihiko Inagawa
Hideyo Hirai
Marcus Fruttiger
Susumu Itoh
Fumiko Itoh
Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression
iScience
Natural sciences
Biological sciences
Systems biology
Cancer systems biology
Cancer
title Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression
title_full Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression
title_fullStr Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression
title_full_unstemmed Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression
title_short Reduced lung metastasis in endothelial cell-specific transforming growth factor β type II receptor-deficient mice with decreased CD44 expression
title_sort reduced lung metastasis in endothelial cell specific transforming growth factor β type ii receptor deficient mice with decreased cd44 expression
topic Natural sciences
Biological sciences
Systems biology
Cancer systems biology
Cancer
url http://www.sciencedirect.com/science/article/pii/S2589004224027299
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