Fibroblast-derived CXCL12 promotes breast cancer metastasis by facilitating tumor cell intravasation

Ahirwar, Dinesh K.; Nasser, Mohd W.; Ouseph, Madhu M.; Elbaz, Mohamad; Cuitiño, Maria C.; Kladney, Raleigh D.; Varikuti, Sanjay; Kaul, Kirti; Satoskar, Abhay R.; Ramaswamy, Bhuvaneswari; Zhang, Xiaoli; Ostrowski, Michael C.; Leone, Gustavo; Ganju, Ramesh K.

doi:10.1038/s41388-018-0263-7

Cited by 165Chemokine receptors and signalingAngiogenesis and VEGF in CancerCancer Cells and Metastasis

Fibroblast-derived CXCL12 promotes breast cancer metastasis by facilitating tumor cell intravasation

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Ahirwar, Dinesh K., Nasser, Mohd W., Ouseph, Madhu M., Elbaz, Mohamad, Cuitiño, Maria C., Kladney, Raleigh D., Varikuti, Sanjay, Kaul, Kirti +6 more·2018·Oncogene

DOI 10.1038/s41388-018-0263-7PMC PMC7063845

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Abstract

The chemokine CXCL12 has been shown to regulate breast tumor growth, however, its mechanism in initiating distant metastasis is not well understood. Here, we generated a novel conditional allele of Cxcl12 in mice and used a fibroblast-specific Cre transgene along with various mammary tumor models to evaluate CXCL12 function in the breast cancer metastasis. Ablation of CXCL12 in stromal fibroblasts of mice significantly delayed the time to tumor onset and inhibited distant metastasis in different mouse models. Elucidation of mechanisms using in vitro and in vivo model systems revealed that CXCL12 enhances tumor cell intravasation by increasing vascular permeability and expansion of a leaky tumor vasculature. Furthermore, our studies revealed CXCL12 enhances permeability by recruiting endothelial precursor cells and decreasing endothelial tight junction and adherence junction proteins. High expression of stromal CXCL12 in large cohort of breast cancer patients was directly correlated to blood vessel density and inversely correlated to recurrence and overall patient survival. In addition, our analysis revealed that stromal CXCL12 levels in combination with number of CD31+ blood vessels confers poorer patient survival compared to individual protein level. However, no correlation was observed between epithelial CXCL12 and patient survival or blood vessel density. Our findings describe the novel interactions between fibroblasts-derived CXCL12 and endothelial cells in facilitating tumor cell intrvasation, leading to distant metastasis. Overall, our studies indicate that cross-talk between fibroblast-derived CXCL12 and endothelial cells could be used as novel biomarker and strategy for developing tumor microenvironment based therapies against aggressive and metastatic breast cancer.

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Various observations highlight activities of TGF-β on endothelial cells that may promote or repress angiogenesis, depending on the experimental setting.
“Various observations highlight activities of TGF-β on endothelial cells that may promote or repress angiogenesis, depending on the experimental setting264–266.”
From TGFβ biology in cancer progression and immunotherapy (2021) · cites this paper as [264]

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CXCL12 regulates breast cancer metastasis and T lymphocyte infiltrationPreprint
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CXCL12 promotes CCR7 ligand–mediated breast cancer cell invasion and migration toward lymphatic vessels
Hayasaka, H., Yoshida, J., Kuroda, Y., Nishiguchi, A., Matsusaki, M., Kishimoto, K., Nishimura, H., Okada, M., Shimomura, Y., Kobayashi, D., et al. (2022) · Cancer Science · doi:10.1111/cas.15293 · Cited by 29 · see citing works

Authors: Ahirwar, D. K., Nasser, M. W., Ouseph, M. M., Elbaz, M., Cuitiño, M. C., Kladney, R. D., Varikuti, S., Kaul, K., Satoskar, A. R., Ramaswamy, B., Zhang, X., Ostrowski, M. C., Leone, G., & Ganju, R. K.
Affiliations: The Ohio State University (US)
Corresponding author: Leone, Gustavo
Ganju, Ramesh K.
ORCID: Ahirwar, Dinesh K.
Nasser, Mohd W.
Ouseph, Madhu M.
Satoskar, Abhay R.
Ramaswamy, Bhuvaneswari
Zhang, Xiaoli
Ostrowski, Michael C.
Leone, Gustavo
Ganju, Ramesh K.
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2018-05-03
Volume: 37
Issue: 32
Pages: 4428-4442
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/s41388-018-0263-7
PMC: PMC7063845
OpenAlex: W2800801906
Cited by: 162
References: 36
Citations by year: 2026: 15 · 2025: 17 · 2024: 35 · 2023: 12 · 2022: 13 · 2021: 23 · 2020: 18 · 2019: 17 · 2018: 12
FWCI: 6.58
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: U.S. Department of Defense
Ohio State University
Pelotonia
National Cancer Institute (R01CA153490, R01CA109527, P01CA097189)
Topics: Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: CXCL12, breast cancer metastasis, tumor cell intravasation, tumor stromal fibroblasts, vascular permeability, tumor vasculature, endothelial progenitor cells, endothelial tight junctions, blood vessel density, patient survival, tumor microenvironment, conditional alleles
MeSH terms: Animals, Breast Neoplasms, Cell Line, Cell Movement, Female, Fibroblasts, Mice, Transgenic, Neoplasm Invasiveness, Neoplasm Metastasis, Mammary Neoplasms, Animal, Endothelial Cells, Cell Line, Tumor, Mice, Chemokine CXCL12, Tumor Microenvironment

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Fibroblast-derived CXCL12 promotes breast cancer metastasis by facilitating tumor cell intravasation

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