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Science 306 (5693): 120-124

Copyright © 2004 by the American Association for the Advancement of Science

Regulation of Cytokine Receptors by Golgi N-Glycan Processing and Endocytosis

Emily A. Partridge,1,3 Christine Le Roy,1 Gianni M. Di Guglielmo,1 Judy Pawling,1 Pam Cheung,1,2 Maria Granovsky,1,2 Ivan R. Nabi,4 Jeffrey L. Wrana,1,2 James W. Dennis1,2,3*

Abstract: The Golgi enzyme ß1,6 N-acetylglucosaminyltransferase V (Mgat5) is up-regulated in carcinomas and promotes the substitution of N-glycan with poly N-acetyllactosamine, the preferred ligand for galectin-3 (Gal-3). Here, we report that expression of Mgat5 sensitized mouse cells to multiple cytokines. Gal-3 cross-linked Mgat5-modified N-glycans on epidermal growth factor and transforming growth factor–ß receptors at the cell surface and delayed their removal by constitutive endocytosis. Mgat5 expression in mammary carcinoma was rate limiting for cytokine signaling and consequently for epithelial-mesenchymal transition, cell motility, and tumor metastasis. Mgat5 also promoted cytokine-mediated leukocyte signaling, phagocytosis, and extravasation in vivo. Thus, conditional regulation of N-glycan processing drives synchronous modification of cytokine receptors, which balances their surface retention against loss via endocytosis.

1 Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, ON M5G 1X5, Canada.
2 Department of Medical Genetics and Microbiology, University of Toronto, Toronto, ON M5S 1A8, Canada.
3 Department of Laboratory Medicine and Pathology, University of British Columbia, Vancouver, BC V6T 1Z3, Canada.
4 Department of Anatomy, Cell Biology, and Physiology,

* To whom correspondence should be addressed. E-mail: Dennis{at}mshri.on.ca

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Intracellular sorting of galectin-8 based on carbohydrate fine specificity.
S. Carlsson, M. C Carlsson, and H. Leffler (2007)
Glycobiology 17, 906-912
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A Galectin of Unique Domain Organization from Hemocytes of the Eastern Oyster (Crassostrea virginica) Is a Receptor for the Protistan Parasite Perkinsus marinus.
S. Tasumi and G. R. Vasta (2007)
J. Immunol. 179, 3086-3098
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Kinetics of mobilization and differentiation of lymphohematopoietic cells during experimental murine schistosomiasis in galectin-3 / mice.
F. L. Oliveira, P. Frazao, R. Chammas, D. K. Hsu, F. T. Liu, R. Borojevic, C. M. Takiya, and M. C. El-Cheikh (2007)
J. Leukoc. Biol. 82, 300-310
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Metabolic homeostasis and tissue renewal are dependent on {beta}1,6GlcNAc-branched N-glycans.
P. Cheung, J. Pawling, E. A Partridge, B. Sukhu, M. Grynpas, and J. W Dennis (2007)
Glycobiology 17, 828-837
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Inhibition of a Specific N-Glycosylation Activity Results in Attenuation of Breast Carcinoma Cell Invasiveness-related Phenotypes: INHIBITION OF EPIDERMAL GROWTH FACTOR-INDUCED DEPHOSPHORYLATION OF FOCAL ADHESION KINASE.
H.-B. Guo, M. Randolph, and M. Pierce (2007)
J. Biol. Chem. 282, 22150-22162
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Control of T Cell-mediated Autoimmunity by Metabolite Flux to N-Glycan Biosynthesis.
A. Grigorian, S.-U. Lee, W. Tian, I.-J. Chen, G. Gao, R. Mendelsohn, J. W. Dennis, and M. Demetriou (2007)
J. Biol. Chem. 282, 20027-20035
   Abstract »    Full Text »    PDF »
Mgat5 and Pten interact to regulate cell growth and polarity.
P. Cheung and J. W. Dennis (2007)
Glycobiology 17, 767-773
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Introduction of bisecting GlcNAc in N-glycans of adenylyl cyclase III enhances its activity.
W. Li, M. Takahashi, Y. Shibukawa, S. Yokoe, J. Gu, E. Miyoshi, K. Honke, Y. Ikeda, and N. Taniguchi (2007)
Glycobiology 17, 655-662
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The Asn418-Linked N-Glycan of ErbB3 Plays a Crucial Role in Preventing Spontaneous Heterodimerization and Tumor Promotion.
S. Yokoe, M. Takahashi, M. Asahi, S. H. Lee, W. Li, D. Osumi, E. Miyoshi, and N. Taniguchi (2007)
Cancer Res. 67, 1935-1942
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Mass Spectrometry Analysis of the Native Protein Complex Containing Actinin-4 in Prostate Cancer Cells.
T. Hara, K. Honda, M. Shitashige, M. Ono, H. Matsuyama, K. Naito, S. Hirohashi, and T. Yamada (2007)
Mol. Cell. Proteomics 6, 479-491
   Abstract »    Full Text »    PDF »
Visualization of Galectin-3 Oligomerization on the Surface of Neutrophils and Endothelial Cells Using Fluorescence Resonance Energy Transfer.
J. Nieminen, A. Kuno, J. Hirabayashi, and S. Sato (2007)
J. Biol. Chem. 282, 1374-1383
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N-Acetylglucosaminyltransferase III Antagonizes the Effect of N-Acetylglucosaminyltransferase V on {alpha}3beta1 Integrin-mediated Cell Migration.
Y. Zhao, T. Nakagawa, S. Itoh, K.-i. Inamori, T. Isaji, Y. Kariya, A. Kondo, E. Miyoshi, K. Miyazaki, N. Kawasaki, et al. (2006)
J. Biol. Chem. 281, 32122-32130
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Intracellular Retention, Degradation, and Signaling of Glycosylation-deficient FGFR2 and Craniosynostosis Syndrome-associated FGFR2C278F.
N. E. Hatch, M. Hudson, M. L. Seto, M. L. Cunningham, and M. Bothwell (2006)
J. Biol. Chem. 281, 27292-27305
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Comparative Analysis by Frontal Affinity Chromatography of Oligosaccharide Specificity of GlcNAc-Binding Lectins, Griffonia simplicifolia Lectin-II (GSL-II) and Boletopsis leucomelas Lectin (BLL).
S. Nakamura-Tsuruta, J. Kominami, M. Kamei, Y. Koyama, T. Suzuki, M. Isemura, and J. Hirabayashi (2006)
J. Biochem. 140, 285-291
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Galectin Binding to Mgat5-Modified N-Glycans Regulates Fibronectin Matrix Remodeling in Tumor Cells.
A. Lagana, J. G. Goetz, P. Cheung, A. Raz, J. W. Dennis, and I. R. Nabi (2006)
Mol. Cell. Biol. 26, 3181-3193
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Chemical Enhancers of Cytokine Signaling that Suppress Microfilament Turnover and Tumor Cell Growth..
H.-J. Park, E. Partridge, P. Cheung, J. Pawling, R. Donovan, J. L. Wrana, and J. W. Dennis (2006)
Cancer Res. 66, 3558-3566
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Complex N-glycans are the major ligands for galectin-1, -3, and -8 on Chinese hamster ovary cells.
S. K. Patnaik, B. Potvin, S. Carlsson, D. Sturm, H. Leffler, and P. Stanley (2006)
Glycobiology 16, 305-317
   Abstract »    Full Text »    PDF »

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