Skip to main content

Identification of Endothelial Cell Surface Carbohydrate-Binding Receptors by Carbohydrate Ligand Mimicry Peptides

  • 1272 Accesses

Part of the Advances in Experimental Medicine and Biology book series (volume 749)

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.

Keywords

  • Splice Factor
  • Endothelial Cell Surface
  • Lung Colonization
  • Endothelial Receptor
  • Lung Endothelial Cell

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-1-4614-3381-1_5
  • Chapter length: 10 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   169.00
Price excludes VAT (USA)
  • ISBN: 978-1-4614-3381-1
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   219.99
Price excludes VAT (USA)
Hardcover Book
USD   279.99
Price excludes VAT (USA)
Fig. 5.1
Fig. 5.2
Fig. 5.3
Fig. 5.4
Fig. 5.5
Fig. 5.6

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Filipenko NR, MacLeod TJ, Yoon CS, Waisman DM (2004) Annexin A2 is a novel RNA-binding protein. J Biol Chem 279:8723–8731

    PubMed  CrossRef  CAS  Google Scholar 

  • Fukuda M (1996) Possible roles of tumor-associated carbohydrate antigens. Cancer Res 56:2237–2244

    PubMed  CAS  Google Scholar 

  • Fukuda MN, Yoneyama T (2010) Identification of carbohydrate-binding proteins by carbohydrate mimicry peptides. Methods Enzymol 478:563–572

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Hakomori S (1985) Aberrant glycosylation in cancer cell membranes as focused on glycolipids: overview and perspectives. Cancer Res 45:2405–2414

    PubMed  CAS  Google Scholar 

  • Hakomori S (2002) Glycosylation defining cancer malignancy: new wine in an old bottle. Proc Natl Acad Sci USA 99:10231–10233

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Haudek KC, Patterson RJ, Wang JL (2010) SR proteins and galectins: what’s in a name? Glycobiology 20:1199–1207

    Google Scholar 

  • Hirata A, Hirata F (1999) Lipocortin (Annexin) I heterotetramer binds to purine RNA and pyrimidine DNA. Biochem Biophys Res Commun 265:200–204

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Irimura T (1994) Cancer metastasis determined by carbohydrate-mediated cell adhesion. Adv Exp Med Biol 353:27–34

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Kannagi R (1997) Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj J 14:577–584

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Liu F, Patterson R, Wang J (2002) Intracellular functions of galectins. Biochim Biophys Acta 1572:263

    PubMed  CrossRef  CAS  Google Scholar 

  • Malisan F, Testi R (2002) GD3 ganglioside and apoptosis. Biochim Biophys Acta 1585:179–187

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Pytela R, Pierschbacher MD, Argraves S, Ruoslahti E (1987) Arginine-glycine-asparatic acid adhesion receptors. Methods Enzymol 144:475–489

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Wang JL, Gray RM, Haudek KC, Patterson RJ (2004) Nucleocytoplasmic lectins. Biochim Biophys Acta 1673:75–93

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michiko N. Fukuda .

Editor information

Editors and Affiliations

Rights and permissions

Reprints 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