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MUC1 Mediates Transendothelial Migration in vitro by Ligating Endothelial Cell ICAM-1

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Abstract

MUC1 is a transmembrane glycoprotein expressed by normal breast epithelium and virtually all breast cancers. MUC1 is normally restricted to the apical surface of epithelia and loss of this polarized distribution in breast carcinomas is associated with lymph node metatases. Our previous work found that MUC1 can bind intercellular adhesion molecule-1 (ICAM-1), mediating adhesion of breast cancer cells to a simulated blood vessel wall, and also triggering a calcium-based signal in the MUC1-bearing cells. It is possible that the depolarized membrane distribution of MUC1 in breast carcinomas may facilitate interactions with stromal/endothelial ICAM-1 leading to adhesion and subsequent migration through the vessel wall. In the current study, we provide evidence that ICAM-1 can influence the migration of cells that express endogenous or transfected MUC1. Migration across a gelatin-coated Transwell membrane could be increased in a step-wise manner by the sequential addition of ICAM-1-expressing cells (endothelial cells and fibroblasts), and ICAM-1-inducing inflammatory cytokines (tumour necrosis factor-α and interleukin-1β). Antibodies against MUC1 or ICAM-1, but not a control antibody, could abrogate migratory increases. Cells that did not express MUC1 were unresponsive to ICAM-1. Our current findings build on our earlier work, by suggesting that the end result of the MUC1/ICAM-1-mediated cell–cell adhesion and calcium-based signal is migration. This has implications for the exit of circulating tumour cells from the vasculature, as well as tumour cell migration through fibroblast-containing stroma underlying the endothelial wall.

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Abbreviations

DMEM:

Dulbecco’s minimal essential medium

DPBS:

Dulbecco’s phosphate buffered saline

ECGS:

endothelial cell growth supplement

ECL:

enhanced chemiluminescence

EGFR:

epidermal growth factor receptor

ERK:

extracellular signal-regulated kinase

FBS:

fetal bovine serum

Grb2:

growth factor receptor-bound protein 2

GSK3 β :

glycogen synthase kinase-3β

HMEC:

human mammary epithelial cell

HUVEC:

human umbilical vein endothelial cell

ICAM-1:

intercellular adhesion molecule-1

IGF:

insulin-like growth factor

IL-1β :

interleukin-1β

LCA:

leukocyte common antigen

MAPK:

mitogen activated protein kinase

MIP-1:

macrophage inflammatory protein 1

NBT/BCIP:

nitroblue tetrazolium chloride/5-bromo-4-chloro-3-indolyl phosphate, toluidine salt

PCNA:

proliferating cell nuclear antigen

PHEC:

primary human endothelial cell

PI3-kinase:

phosphoinositol-3-kinase

PKCδ:

protein kinase C δ

RANTES:

regulated upon activation, normal T-cell expressed and secreted

sc-uPA:

single-chain urokinase-type plasminogen activator

SEM:

standard error of the mean

Sos:

son of sevenless

SYM:

signal sequence-YFP-MUC1

TEME :

transendothelial migration, specifically extravasation

TNF-α :

tumour necrosis factor α

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Authors and Affiliations

  1. Department of Laboratory Medicine and Pathology, Cross Cancer Institute, University of Alberta, Edmonton, AB, Canada

    Jennifer J. Rahn, Jeffrey W. Chow, Garnet J. Horne, Brian K. Mah & Judith C. Hugh

  2. Department of Cellular & Physiological Sciences, Faculty of Medicine, University of British Colombia, Vancouver, BC, Canada

    Joanne T. Emerman

  3. ICOS Corporation, Bothell, Washington, USA

    Pat Hoffman

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  1. Jennifer J. Rahn
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  2. Jeffrey W. Chow
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  3. Garnet J. Horne
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  7. Judith C. Hugh
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Correspondence to Judith C. Hugh.

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Rahn, J.J., Chow, J.W., Horne, G.J. et al. MUC1 Mediates Transendothelial Migration in vitro by Ligating Endothelial Cell ICAM-1. Clin Exp Metastasis 22, 475–483 (2005). https://doi.org/10.1007/s10585-005-3098-x

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