Abstract
American women have a nearly 25% lifetime risk of developing breast cancer, with 20% to 40% of these patients developing life-threatening metastases. More than 70% of patients presenting with metastases have skeletal involvement, which signals progression to an incurable stage. Tumor-stroma cell interactions are only superficially understood, specifically regarding the ability of stromal cells to affect metastasis. In vivo models show that exogenously supplied human bone marrow-derived stem cells (hBMSC) migrate to breast cancer tumors, but no reports have shown endogenous hBMSC migration from the bone to primary tumors. Here, we present a model of in vivo hBMSC migration from a physiologic human bone environment to human breast tumors. Furthermore, hBMSCs alter tumor growth and bone metastasis frequency. These may home to certain breast tumors based on tumor-derived TGF-β1. Moreover, at the primary tumor level, interleukin 17B (IL-17B)/IL-17BR signaling may mediate interactions between hBMSCs and breast cancer cells.
MeSH Terms
Animals
Bone Marrow Cells/pathology
Bone Neoplasms/secondary
Breast Neoplasms/genetics,metabolism,pathology
Carcinoma, Ductal, Breast/pathology,secondary
Cell Communication/physiology
Cell Line, Tumor
Female
Gene Expression Profiling
Humans
Interleukin-17/biosynthesis,genetics,physiology
Mesenchymal Stem Cells/pathology
Mice
Mice, Inbred NOD
Mice, SCID
Receptors, Interleukin-17/metabolism
Reverse Transcriptase Polymerase Chain Reaction
Stromal Cells/pathology
Transforming Growth Factor beta/antagonists & inhibitors,metabolism,physiology
Transplantation, Heterologous
Chemicals
Interleukin-17
Receptors, Interleukin-17
Transforming Growth Factor beta
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Goldstein Robert H
Program in Genetics, Sackler School of Biomedical Sciences, Tufts University, Boston, Massachusetts, USA.
Reagan Michaela R
Anderson Kristen
Kaplan David L
Rosenblatt Michael
References (21)
21 references, click to expand
-
IL-17 stimulates the proliferation and differentiation of human mesenchymal stem cells: implications for bone remodeling.
Cell Death Differ. 2009 Oct;16(10):1332-43
PMID: 19543237
-
Reconstruction of human mammary tissues in a mouse model.
Nat Protoc. 2006;1(1):206-14
PMID: 17406234
-
Matrix-mediated retention of adipogenic differentiation potential by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion.
Biomaterials. 2005 Nov;26(31):6167-75
PMID: 15913765
-
Functional culture models to study mechanisms governing apoptosis in normal and malignant mammary epithelial cells.
J Mammary Gland Biol Neoplasia. 1999 Apr;4(2):193-201
PMID: 10426398
-
Cancer statistics, 2009.
CA Cancer J Clin. 2009 Jul-Aug;59(4):225-49
PMID: 19474385
-
The Snf1-related kinase, Hunk, is essential for mammary tumor metastasis.
Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15855-60
PMID: 19717424
-
TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation.
Nat Med. 2009 Jul;15(7):757-65
PMID: 19584867
-
Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment.
Cancer Res. 2007 Dec 15;67(24):11687-95
PMID: 18089798
-
Concise review: adult multipotent stromal cells and cancer: risk or benefit?
Stem Cells. 2008 Jun;26(6):1387-94
PMID: 18388305
-
Mesenchymal stem cells within tumour stroma promote breast cancer metastasis.
Nature. 2007 Oct 4;449(7162):557-63
PMID: 17914389
-
Human mesenchymal stem cells induce E-cadherin degradation in breast carcinoma spheroids by activating ADAM10.
Cell Mol Life Sci. 2009 Sep;66(18):3053-65
PMID: 19603142
-
Phorbol ester induced osteoclast-like differentiation of a novel human leukemic cell line (FLG 29.1).
J Cell Biol. 1992 Jan;116(2):437-47
PMID: 1309813
-
A multigenic program mediating breast cancer metastasis to bone.
Cancer Cell. 2003 Jun;3(6):537-49
PMID: 12842083
-
Clinical management of women with metastatic breast cancer: a descriptive study according to age group.
BMC Cancer. 2006 Jul 06;6:179
PMID: 16824210
-
Genomic predictors of outcome and treatment response in breast cancer.
Mol Diagn Ther. 2009;13(2):73-90
PMID: 19537843
-
Malignant cells, directors of the malignant process: role of transforming growth factor-beta.
Cancer Metastasis Rev. 2001;20(1-2):133-43
PMID: 11831642
-
Analysis of the expression profiles of cytokines and cytokine-related genes during the progression of breast cancer growth in mice.
Oncol Rep. 2009 Nov;22(5):1141-7
PMID: 19787232
-
Tissue-engineered bone serves as a target for metastasis of human breast cancer in a mouse model.
Cancer Res. 2007 Nov 1;67(21):10304-8
PMID: 17974972
-
Immunolocalization of IL-17A, IL-17B, and their receptors in chondrocytes during fracture healing.
J Histochem Cytochem. 2008 Feb;56(2):89-95
PMID: 17827167
-
A mouse model of human breast cancer metastasis to human bone.
Cancer Res. 2005 Jul 15;65(14):6130-8
PMID: 16024614
-
Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT).
Breast Cancer Res Treat. 2010 Nov;124(2):317-26
PMID: 20087650