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First published online 1 September 2005
doi: 10.1242/jcs.02538

Journal of Cell Science 118, 4175-4185 (2005)
Published by The Company of Biologists 2005
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Research Article

pH-specific sequestration of phosphoglucose isomerase/autocrine motility factor by fibronectin and heparan sulphate

Annick Lagana1, Jacky G. Goetz1,3, Nathalie Y3, Yoram Altschuler2 and Ivan R. Nabi1,3,*

1 Département de pathologie et biologie cellulaire, Université de Montréal, Montréal, Québec, H3C 3J7, Canada
2 Department of Pharmacology, Hebrew University of Jerusalem, Jerusalem 91120, Israel
3 Department of Cellular and Physiological Sciences, University of British Columbia, Vancouver, British Columbia, V6T 1Z3, Canada

* Author for correspondence (e-mail: irnabi{at}interchange.ubc.ca)

Accepted 10 June 2005

Phosphoglucose isomerase (PGI) is a glycolytic enzyme that moonlights as a cytokine under the aliases autocrine motility factor (AMF), neuroleukin and maturation factor. The cytokine function of PGI/AMF targets multiple cell types however mechanisms that regulate and sequester this ubiquitous, circulating cytokine remain largely unidentified. PGI/AMF is shown here to exhibit fibronectin (FN)-dependent cell surface association at both neutral and acid pH. Direct PGI/AMF binding to FN and fluorescence resonance energy transfer (FRET) between PGI/AMF and FN were detected only at pH 5. At neutral pH, the interaction of PGI/AMF with FN is receptor-mediated requiring prior clathrin-dependent endocytosis. PGI/AMF and FN do not co-internalize and PGI/AMF undergoes a second round of endocytosis upon recycling to the plasma membrane indicating that recycling PGI/AMF receptor complexes associate with FN fibrils. Heparan sulphate does not affect cell association of PGI/AMF at neutral pH but enhances the FN-independent cell surface association of PGI/AMF at acid pH identifying two distinct mechanisms for PGI/AMF sequestration under acidic conditions. However, only PGI/AMF sequestration by FN at acid pH was able to stimulate cell motility upon pH neutralization identifying FN as a pH-dependent cytokine trap for PGI/AMF. The multiple ways of cellular association of PGI/AMF may represent acquired mechanisms to regulate and harness the cytokine function of PGI/AMF.

Key words: Cytokine sequestration, Cell motility, Extracellular matrix


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© The Company of Biologists Ltd 2005