Breast Cancer Research and Treatment 63: 105–115, 2000.
© 2000 Kluwer Academic Publishers. Printed in the Netherlands.
Report
Induction of matrix metalloproteinases MMP-1 and MMP-2 by co-culture
of breast cancer cells and bone marrow fibroblasts
Sonia Saad, Linda J Bendall, Alexander James, David J Gottlieb, and Kenneth F Bradstock
Institute for Cancer Research, Westmead Millennium Institute, Westmead Hospital and Faculty of Medicine,
University of Sydney, Sydney, Australia
Key words: bone marrow fibroblasts, breast cancer, migration, matrix metalloproteinases, MMP-1, MMP-2
Summary
Two invasive breast cancer cell lines (MDA-MB-231 and BT-549) were found to be more adherent and have
greater migratory capacity on bone marrow fibroblasts than three non-invasive cell lines (MCF-7, T47D and BT-
483). Antibodies to the adhesion molecules CD44, E-cadherin, ICAM-1, and integrin chains α2, α3, α4, α5, α6,
αv, β1, β3 and β7 failed to inhibit breast cancer cell migration through bone marrow fibroblasts. Inhibitors of
matrix metalloproteases, 1, 10-phenanthroline, Ro-9790, TIMP-1 and TIMP-2 were able to attenuate the migration
of MDA-MB-231 cells through bone marrow fibroblast monolayers suggesting a role for these enzymes in the
migration of breast cancer cells through bone marrow adherent layers. Co-culture of MDA-MB-231 cells and
bone marrow fibroblasts resulted in augmentation of the levels of the matrix metalloproteases MMP-1 and MMP-2
in culture supernatants. Soluble factors produced by bone marrow fibroblasts were responsible for the increase
in MMP-1 levels. However, maximal MMP-2 production was dependent on direct contract between the breast
cancer cells and the bone marrow fibroblasts. Modulation of MMP production by cell–cell contact or soluble
factors suggests a mechanism by which breast cancer cells can enhance their ability to invade the bone marrow
microenvironment.
Introduction
Breast cancer is one of the most common forms of
cancer in women but despite being responsive to hor-
monal manipulation and chemotherapy, relapse fol-
lowing treatment is common, particularly in patients
with metastatic disease [1]. Encouraging results have
been obtained using autologous hematopoietic stem
cell transplantation to facilitate chemotherapy dose in-
tensification for the treatment of metastatic and node-
positive breast cancers [2]. Breast cancers frequently
metastasize to the bone marrow, suggesting that the
marrow may provide a favorable microenvironment
for the growth of tumor cells and act as a reservoir
of disease allowing further hematogenous spread. The
presence of breast cancer cells in the bone marrow
has raised concerns about malignant cell contamina-
tion of reinfused marrow and peripheral blood stem
cell preparations [3].
Matrix metalloproteases (MMPs) are a family of
zinc dependent enzymes with the capacity to degrade
extracellular matrix proteins [4]. MMP expression
has a strong correlation with cancer cell invasiveness
and metastasis [5–7]. Although some MMPs such as
MMP-2 are elevated in breast cancer epithelial cells,
most tumor associated metalloprotease activity occurs
in the adjacent fibroblasts [8]. This suggests that the
MMP activity of non-malignant tissue is modulated by
the adjacent malignant epithelial cells. Similarly, some
MMPs, including MMP-1 and MMP-9 can be induced
in malignant cells by cytokines [9–14]. Crosslinking
of antibodies to the β1 integrins VLAs-2 and -3 can
induce increased production of pro- and active forms
of MMP-2 [15].
We have examined the adhesive interactions
between breast cancer cells and bone marrow derived
fibroblasts and the ability of breast cancer cells to mi-
grate through bone marrow stromal layers. Although
the adhesive mechanisms used by breast cancer cells
to bind to bone marrow fibroblast monolayers are not
clear, it is apparent that MMPs play a role in the migra-
tion of invasive breast cancer cells through monolayers