Leukocyte Complexity Predicts Breast Cancer Survival and Functionally Regulates Response to Chemotherapy
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Abstract
Immune-regulated pathways influence multiple aspects of cancer development. In this article we demonstrate that both macrophage abundance and T-cell abundance in breast cancer represent prognostic indicators for recurrence-free and overall survival. We provide evidence that response to chemotherapy is in part regulated by these leukocytes; cytotoxic therapies induce mammary epithelial cells to produce monocyte/macrophage recruitment factors, including colony stimulating factor 1 (CSF1) and interleukin-34, which together enhance CSF1 receptor (CSF1R)–dependent macrophage infiltration. Blockade of macrophage recruitment with CSF1R-signaling antagonists, in combination with paclitaxel, improved survival of mammary tumor–bearing mice by slowing primary tumor development and reducing pulmonary metastasis. These improved aspects of mammary carcinogenesis were accompanied by decreased vessel density and appearance of antitumor immune programs fostering tumor suppression in a CD8+ T-cell–dependent manner. These data provide a rationale for targeting macrophage recruitment/response pathways, notably CSF1R, in combination with cytotoxic therapy, and identification of a breast cancer population likely to benefit from this novel therapeutic approach. Significance: These findings reveal that response to chemotherapy is in part regulated by the tumor immune microenvironment and that common cytotoxic drugs induce neoplastic cells to produce monocyte/macrophage recruitment factors, which in turn enhance macrophage infiltration into mammary adenocarcinomas. Blockade of pathways mediating macrophage recruitment, in combination with chemotherapy, significantly decreases primary tumor progression, reduces metastasis, and improves survival by CD8+ T-cell–dependent mechanisms, thus indicating that the immune microenvironment of tumors can be reprogrammed to instead foster antitumor immunity and improve response to cytotoxic therapy. Cancer Discovery; 1(1); 54–67. ©2011 AACR. This article is highlighted in the In This Issue feature, p. 4
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In tumor tissues, ECM offers a mechanical supporting scaffold and cell-adhesive proteins and serves as a reservoir for growth factors essential to cancer growth, invasion, and metastasis.
“In tumor tissues, the ECM offers a mechanical supporting scaffold and cell‐adhesive proteins for cellular components and serves as a reservoir for growth factors essential to cancer growth, invasion, and metastasis.[ 32 ]”
From 3D Biomimetic Models to Reconstitute Tumor Microenvironment In Vitro: Spheroids, Organoids, and Tumor‐on‐a‐Chip (2023) · cites this paper as [32]
The Introduction discusses tumor-associated macrophages and their role in invasion and metastasis, not the extracellular matrix. Searches for an ECM scaffold, cell-adhesive proteins, and an ECM reservoir of growth factors found no passage in our copy addressing those claims. (LLM, conf=0.75)
Experimental — accuracy not yet measuredRecent evidence points to tumor microenvironment components as potential participants in the generation of chemoresistance.
“Recent evidence points to tumor microenvironment components as potential participants in the generation of chemoresistance (Denardo et al., 2011; Gilbert and Hemann, 2010; Roodhart et al., 2011; Shaked et al., 2008; Shree et al., 2011).”
From A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis (2012) · cites this paper as Denardo et al., 2011
The critical role of the microenvironment in tumor progression and therapy response is increasingly recognized.
“The critical role of the microenvironment in tumor progression and response to therapy is being increasingly recognized (Condeelis and Pollard, 2006; Denardo et al., 2011; Gilbert and Hemann, 2010; Shree et al., 2011; Tan et al., 2011).”
From A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis (2012) · cites this paper as Denardo et al., 2011
Chemotherapy induces a storm of cytokines and chemokines in the tumor microenvironment, many of which may be linked to chemoresistance.
“Recent reports (Denardo et al., 2011; Gilbert and Hemann, 2010) and the present work show that chemotherapy induces a storm of cytokines and chemokines in the tumor microenvironment many of which might be linked to chemoresistance.”
From A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis (2012) · cites this paper as Denardo et al., 2011
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- Authors
- DeNardo, D. G., Brennan, D. J., Rexhepaj, E., Ruffell, B., Shiao, S. L., Madden, S. F., Gallagher, W. M., Wadhwani, N., Keil, S. D., Junaid, S. A., Rugo, H. S., Hwang, E. S., Jirström, K., West, B. L., & Coussens, L. M.
- Affiliations
- University College Dublin (IE)
- ORCID
- Venue
- Cancer Discovery
- Published
- 2011-06-01
- Volume
- 1
- Issue
- 1
- Pages
- 54-67
- ISSN
- 2159-8274 (ISSN-L)
- 2159-8290
- PMC
- PMC3203524
- OpenAlex
- W2163035374
- Cited by
- 1,715
- References
- 66
- Citations by year
- 2026: 29 · 2025: 56 · 2024: 94 · 2023: 129 · 2022: 117 · 2021: 156 · 2020: 126 · 2019: 130 · 2018: 141 · 2017: 125 · 2016: 126 · 2015: 111 · 2014: 144 · 2013: 127 · 2012: 73
- FWCI
- 52.77
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Discovery (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- Lunds Universitet
- Plexxikon
- National Cancer Institute (R01CA132566, R01CA140943, P50CA058207, R01CA130980, P50-CA 58207)
- Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- breast cancer, macrophage recruitment, CSF1R, IL-34, colony-stimulating factor 1, chemotherapy response, paclitaxel, CD8+ T cells, tumor immune microenvironment, antitumor immunity, lung metastasis, tumor vasculature, prognostic factors, combination therapy
- MeSH terms
- Aged, Animals, Breast Neoplasms, Epithelial Cells, Female, Follow-Up Studies, Humans, Leukocytes, Lung Neoplasms, Macrophages, Mammary Neoplasms, Experimental, Neoplasm Metastasis, Prognosis, Cohort Studies, Signal Transduction, Survival Rate, Macrophage Colony-Stimulating Factor, Receptor, Macrophage Colony-Stimulating Factor, Paclitaxel, CD8-Positive T-Lymphocytes, Disease-Free Survival, Mice, Tumor Microenvironment
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