Abstract
Substantial evidence suggests that cell surface carbohydrate antigens, particularly those containing fucose residues, are related to cancer malignancy. To investigate the mechanisms underlying cell surface carbohydrate-dependent cancer metastasis, we developed a 7-mer peptide, designated as I-peptide, which is capable of inhibiting FUT3-transfected B16 cell colonization of lung in the mouse. I-peptide inhibited lung colonization of FUT3-B16 cells in E-/P-selectin doubly deficient mutant mice, suggesting the existence of an as yet unidentified carbohydrate-binding endothelial receptor distinct from E-/P-selectins. Subsequently, we isolated the endothelial receptors by I-peptide affinity chromatography and identified them by proteomics. Thus, I-peptide receptors were identified to be pre-mRNA splicing factor (Sfrs) proteins. We also found a fragment of annexin A1 (Anxa1) bound to I-peptide. Our study demonstrated the usefulness of carbohydrate-ligand mimicry peptide for the identification of novel carbohydrate-binding proteins.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Barondes SH, Cooper DN, Gitt MA, Leffler H (1994) Galectins: structure and function of a large family of animal lectins. J Biol Chem 269:20807–20810
Blixt O, Head S, Mondala T, Scanlan C, Huflejt ME, Alvarez R, Bryan MC, Fazio F, Calarese D, Stevens J et al (2004) Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci USA 101:17033–17038
Borsig L, Wong R, Hynes RO, Varki NM, Varki A (2002) Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci USA 99:2193–2198
Christian S, Pilch J, Akerman ME, Porkka K, Laakkonen P, Ruoslahti E (2003) Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J Cell Biol 163:871–878
De Maria R, Lenti L, Malisan F, d’Agostino F, Tomassini B, Zeuner A, Rippo MR, Testi R (1997) Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science 277:1652–1655
Filipenko NR, MacLeod TJ, Yoon CS, Waisman DM (2004) Annexin A2 is a novel RNA-binding protein. J Biol Chem 279:8723–8731
Fukuda M (1996) Possible roles of tumor-associated carbohydrate antigens. Cancer Res 56:2237–2244
Fukuda MN, Yoneyama T (2010) Identification of carbohydrate-binding proteins by carbohydrate mimicry peptides. Methods Enzymol 478:563–572
Fukuda MN, Ohyama C, Lowitz K, Matsuo O, Pasqualini R, Ruoslahti E, Fukuda M (2000) A peptide mimic of E-selectin ligand inhibits sialyl Lewis X-dependent lung colonization of tumor cells. Cancer Res 60:450–456
Gao-Uozumi CX, Uozumi N, Miyoshi E, Nagai K, Ikeda Y, Teshima T, Noda K, Shiba T, Honke K, Taniguchi N (2000) A novel carbohydrate binding activity of annexin V toward a bisecting N-acetylglucosamine. Glycobiology 10:1209–1216
Hakomori S (1985) Aberrant glycosylation in cancer cell membranes as focused on glycolipids: overview and perspectives. Cancer Res 45:2405–2414
Hakomori S (2002) Glycosylation defining cancer malignancy: new wine in an old bottle. Proc Natl Acad Sci USA 99:10231–10233
Hatakeyama S, Sugihara K, Nakayama J, Akama TO, Wong SM, Kawashima H, Zhang J, Smith DF, Ohyama C, Fukuda M et al (2009) Identification of mRNA splicing factors as the endothelial receptor for carbohydrate-dependent lung colonization of cancer cells. Proc Natl Acad Sci USA 106:3095–3100
Haudek KC, Patterson RJ, Wang JL (2010) SR proteins and galectins: what’s in a name? Glycobiology 20:1199–1207
Hirata A, Hirata F (1999) Lipocortin (Annexin) I heterotetramer binds to purine RNA and pyrimidine DNA. Biochem Biophys Res Commun 265:200–204
Hirata A, Hirata F (2002) DNA chain unwinding and annealing reactions of lipocortin (annexin) I heterotetramer: regulation by Ca(2+) and Mg(2+). Biochem Biophys Res Commun 291:205–209
Horlacher T, Noti C, de Paz JL, Bindschadler P, Hecht ML, Smith DF, Fukuda MN, Seeberger PH (2011) Characterization of annexin A1 glycan binding reveals binding to highly sulfated glycans with preference for highly sulfated heparan sulfate and heparin. Biochemistry 50:2650–2659
Irimura T (1994) Cancer metastasis determined by carbohydrate-mediated cell adhesion. Adv Exp Med Biol 353:27–34
Irimura T, Nakamori S, Matsushita Y, Taniuchi Y, Todoroki N, Tsuji T, Izumi Y, Kawamura Y, Hoff SD, Cleary KR et al (1993) Colorectal cancer metastasis determined by carbohydrate-mediated cell adhesion: role of sialyl-LeX antigens. Semin Cancer Biol 4:319–324
Ishitsuka R, Kojima K, Utsumi H, Ogawa H, Matsumoto I (1998) Glycosaminoglycan binding properties of annexin IV, V, and VI. J Biol Chem 273:9935–9941
Kannagi R (1997) Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj J 14:577–584
Kannagi R, Izawa M, Koike T, Miyazaki K, Kimura N (2004) Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci 95:377–384
Kojima K, Ogawa HK, Seno N, Yamamoto K, Irimura T, Osawa T, Matsumoto I (1992) Carbohydrate-binding proteins in bovine kidney have consensus amino acid sequences of annexin family proteins. J Biol Chem 267:20536–20539
Kojima K, Yamamoto K, Irimura T, Osawa T, Ogawa H, Matsumoto I (1996) Characterization of carbohydrate-binding protein p33/41: relation with annexin IV, molecular basis of the doublet forms (p33 and p41), and modulation of the carbohydrate binding activity by phospholipids. J Biol Chem 271:7679–7685
Liu F, Patterson R, Wang J (2002) Intracellular functions of galectins. Biochim Biophys Acta 1572:263
Malisan F, Testi R (2002) GD3 ganglioside and apoptosis. Biochim Biophys Acta 1585:179–187
Ohyama C, Tsuboi S, Fukuda M (1999) Dual roles of sialyl Lewis X oligosaccharides in tumor metastasis and rejection by natural killer cells. EMBO J 18:1516–1525
Pasqualini R, Koivunen E, Kain R, Lahdenranta J, Sakamoto M, Stryhn A, Ashmun RA, Shapiro LH, Arap W, Ruoslahti E (2000) Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res 60:722–727
Pytela R, Pierschbacher MD, Ruoslahti E (1985) Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell 40:191–198
Pytela R, Pierschbacher MD, Argraves S, Ruoslahti E (1987) Arginine-glycine-asparatic acid adhesion receptors. Methods Enzymol 144:475–489
Rajotte D, Ruoslahti E (1999) Membrane dipeptidase is the receptor for a lung-targeting peptide identified by in vivo phage display. J Biol Chem 274:11593–11598
Srikrishna G, Panneerselvam K, Westphal V, Abraham V, Varki A, Freeze HH (2001) Two proteins modulating transendothelial migration of leukocytes recognize novel carboxylated glycans on endothelial cells. J Immunol 166:4678–4688
Wang JL, Gray RM, Haudek KC, Patterson RJ (2004) Nucleocytoplasmic lectins. Biochim Biophys Acta 1673:75–93
Zhang J, Nakayama J, Ohyama C, Suzuki M, Suzuki A, Fukuda M, Fukuda MN (2002) Sialyl Lewis X-dependent lung colonization of B16 melanoma cells through a selectin-like endothelial receptor distinct from E- or P-selectin. Cancer Res 62:4194–4198
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media, LLC
About this paper
Cite this paper
Fukuda, M.N. (2012). Identification of Endothelial Cell Surface Carbohydrate-Binding Receptors by Carbohydrate Ligand Mimicry Peptides. In: Sudhakaran, P., Surolia, A. (eds) Biochemical Roles of Eukaryotic Cell Surface Macromolecules. Advances in Experimental Medicine and Biology, vol 749. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3381-1_5
Download citation
DOI: https://doi.org/10.1007/978-1-4614-3381-1_5
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-3380-4
Online ISBN: 978-1-4614-3381-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)