Angiotensin II facilitates breast cancer cell migration and metastasis

Breast cancer metastasis is a leading cause of death by malignancy in women worldwide. Efforts are being made to further characterize the rate-limiting steps of cancer metastasis, i.e. extravasation of circulating tumor cells and colonization of secondary organs. In this study, we investigated wheth...

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Published inPloS one Vol. 7; no. 4; p. e35667
Main Authors Rodrigues-Ferreira, Sylvie, Abdelkarim, Mohamed, Dillenburg-Pilla, Patricia, Luissint, Anny-Claude, di-Tommaso, Anne, Deshayes, Frédérique, Pontes, Carmen Lucia S, Molina, Angie, Cagnard, Nicolas, Letourneur, Franck, Morel, Marina, Reis, Rosana I, Casarini, Dulce E, Terris, Benoit, Couraud, Pierre-Olivier, Costa-Neto, Claudio M, Di Benedetto, Mélanie, Nahmias, Clara
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 20.04.2012
Public Library of Science (PLoS)
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Abstract Breast cancer metastasis is a leading cause of death by malignancy in women worldwide. Efforts are being made to further characterize the rate-limiting steps of cancer metastasis, i.e. extravasation of circulating tumor cells and colonization of secondary organs. In this study, we investigated whether angiotensin II, a major vasoactive peptide both produced locally and released in the bloodstream, may trigger activating signals that contribute to cancer cell extravasation and metastasis. We used an experimental in vivo model of cancer metastasis in which bioluminescent breast tumor cells (D3H2LN) were injected intra-cardiacally into nude mice in order to recapitulate the late and essential steps of metastatic dissemination. Real-time intravital imaging studies revealed that angiotensin II accelerates the formation of metastatic foci at secondary sites. Pre-treatment of cancer cells with the peptide increases the number of mice with metastases, as well as the number and size of metastases per mouse. In vitro, angiotensin II contributes to each sequential step of cancer metastasis by promoting cancer cell adhesion to endothelial cells, trans-endothelial migration and tumor cell migration across extracellular matrix. At the molecular level, a total of 102 genes differentially expressed following angiotensin II pre-treatment were identified by comparative DNA microarray. Angiotensin II regulates two groups of connected genes related to its precursor angiotensinogen. Among those, up-regulated MMP2/MMP9 and ICAM1 stand at the crossroad of a network of genes involved in cell adhesion, migration and invasion. Our data suggest that targeting angiotensin II production or action may represent a valuable therapeutic option to prevent metastatic progression of invasive breast tumors.
AbstractList Breast cancer metastasis is a leading cause of death by malignancy in women worldwide. Efforts are being made to further characterize the rate-limiting steps of cancer metastasis, i.e. extravasation of circulating tumor cells and colonization of secondary organs. In this study, we investigated whether angiotensin II, a major vasoactive peptide both produced locally and released in the bloodstream, may trigger activating signals that contribute to cancer cell extravasation and metastasis. We used an experimental in vivo model of cancer metastasis in which bioluminescent breast tumor cells (D3H2LN) were injected intra-cardiacally into nude mice in order to recapitulate the late and essential steps of metastatic dissemination. Real-time intravital imaging studies revealed that angiotensin II accelerates the formation of metastatic foci at secondary sites. Pre-treatment of cancer cells with the peptide increases the number of mice with metastases, as well as the number and size of metastases per mouse. In vitro, angiotensin II contributes to each sequential step of cancer metastasis by promoting cancer cell adhesion to endothelial cells, trans-endothelial migration and tumor cell migration across extracellular matrix. At the molecular level, a total of 102 genes differentially expressed following angiotensin II pre-treatment were identified by comparative DNA microarray. Angiotensin II regulates two groups of connected genes related to its precursor angiotensinogen. Among those, up-regulated MMP2/MMP9 and ICAM1 stand at the crossroad of a network of genes involved in cell adhesion, migration and invasion. Our data suggest that targeting angiotensin II production or action may represent a valuable therapeutic option to prevent metastatic progression of invasive breast tumors.
Breast cancer metastasis is a leading cause of death by malignancy in women worldwide. Efforts are being made to further characterize the rate-limiting steps of cancer metastasis, i.e. extravasation of circulating tumor cells and colonization of secondary organs. In this study, we investigated whether angiotensin II, a major vasoactive peptide both produced locally and released in the bloodstream, may trigger activating signals that contribute to cancer cell extravasation and metastasis. We used an experimental in vivo model of cancer metastasis in which bioluminescent breast tumor cells (D3H2LN) were injected intra-cardiacally into nude mice in order to recapitulate the late and essential steps of metastatic dissemination. Real-time intravital imaging studies revealed that angiotensin II accelerates the formation of metastatic foci at secondary sites. Pre-treatment of cancer cells with the peptide increases the number of mice with metastases, as well as the number and size of metastases per mouse. In vitro, angiotensin II contributes to each sequential step of cancer metastasis by promoting cancer cell adhesion to endothelial cells, trans-endothelial migration and tumor cell migration across extracellular matrix. At the molecular level, a total of 102 genes differentially expressed following angiotensin II pre-treatment were identified by comparative DNA microarray. Angiotensin II regulates two groups of connected genes related to its precursor angiotensinogen. Among those, up-regulated MMP2/MMP9 and ICAM1 stand at the crossroad of a network of genes involved in cell adhesion, migration and invasion. Our data suggest that targeting angiotensin II production or action may represent a valuable therapeutic option to prevent metastatic progression of invasive breast tumors.
Audience Academic
Author Luissint, Anny-Claude
Morel, Marina
Cagnard, Nicolas
Reis, Rosana I
Molina, Angie
Rodrigues-Ferreira, Sylvie
Deshayes, Frédérique
Costa-Neto, Claudio M
di-Tommaso, Anne
Abdelkarim, Mohamed
Couraud, Pierre-Olivier
Casarini, Dulce E
Di Benedetto, Mélanie
Terris, Benoit
Nahmias, Clara
Letourneur, Franck
Dillenburg-Pilla, Patricia
Pontes, Carmen Lucia S
AuthorAffiliation 1 Inserm, Institut Cochin, Paris, France
5 CNRS, UMRS 940, IGM, Paris, France
8 Department of Medicine, Nephrology Division, Federal University of São Paulo, São Paulo, São Paulo, Brazil
4 Université Paris 13, Bobigny, France
3 Université Paris Descartes, Paris, France
7 Department of Physiological Sciences, Federal University of São Carlos, São Carlos, São Paulo, Brazil
Emory University, United States of America
2 CNRS, Paris, France
6 Department of Biochemistry and Immunology, Faculty of Medicine at Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22536420$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2012 Public Library of Science
2012 Rodrigues-Ferreira et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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.
Distributed under a Creative Commons Attribution 4.0 International License
Rodrigues-Ferreira et al. 2012
Copyright_xml – notice: COPYRIGHT 2012 Public Library of Science
– notice: 2012 Rodrigues-Ferreira et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: Rodrigues-Ferreira et al. 2012
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PMCID: PMC3334979
Conceived and designed the experiments: SR-F MdB CN. Performed the experiments: SR-F MA PD-P A-CL AdT FD CLSP AM MM RIR CMC-N MdB. Analyzed the data: SR-F MA PD-P A-CL AdT FD CLSP AM NC FL MM RIR DEC BT P-OC CMC-N MdB CN. Contributed reagents/materials/analysis tools: NC FL BT P-OC. Wrote the paper: SR-F CMC-N CN.
ORCID 0000-0002-9269-020X
0000-0001-6863-370X
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3334979/
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M Bockhorn (ref4) 2007; 8
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Snippet Breast cancer metastasis is a leading cause of death by malignancy in women worldwide. Efforts are being made to further characterize the rate-limiting steps...
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SubjectTerms Adhesion
Angiogenesis
Angiotensin
Angiotensin II
Angiotensin II - physiology
Angiotensinogen
Angiotensins
Animals
Apoptosis Regulatory Proteins - genetics
Apoptosis Regulatory Proteins - metabolism
Biochemistry
Biology
Bone Neoplasms - secondary
Brain Neoplasms - secondary
Breast cancer
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer
Cancer metastasis
Cell adhesion
Cell adhesion & migration
Cell Adhesion - genetics
Cell Line, Tumor
Cell migration
Cell Proliferation
Cloning
Coculture Techniques
Collaboration
Colonization
Deoxyribonucleic acid
Development and progression
DNA
DNA microarrays
Endothelial cells
Endothelium
Enzymes
Extracellular matrix
Extravasation
Female
Gelatinase A
Gelatinase B
Gene Expression Profiling
Gene Expression Regulation, Neoplastic
Gene Regulatory Networks
Genes
Hostages
Humans
Immunology
Intercellular adhesion molecule 1
Invasiveness
Kinases
Life Sciences
Lung Neoplasms - secondary
Malignancy
Matrix Metalloproteinase 2 - genetics
Matrix Metalloproteinase 2 - metabolism
Matrix Metalloproteinase 9 - genetics
Matrix Metalloproteinase 9 - metabolism
Medical prognosis
Medicine
Meta-analysis
Metastases
Metastasis
Mice
Mice, Nude
Neoplasm Transplantation
Organs
Transendothelial and Transepithelial Migration - genetics
Tumor cells
Tumors
Vasoactive agents
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Title Angiotensin II facilitates breast cancer cell migration and metastasis
URI https://www.ncbi.nlm.nih.gov/pubmed/22536420
https://www.proquest.com/docview/1324596666
https://search.proquest.com/docview/1010236976
https://u-paris.hal.science/hal-03654673
https://pubmed.ncbi.nlm.nih.gov/PMC3334979
https://doaj.org/article/080dd26831f04bd1855e2d4ec677f9ea
http://dx.doi.org/10.1371/journal.pone.0035667
Volume 7
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