Antitumor Activity of Glycosylated Molluscan Hemocyanins via Guerin Ascites Tumor

REFERENCES

• Arcangeli, A., Lucio Toma, L., Contiero, L., Crociani, O.. Legnani, L., Lungh, C., Nesti, E., Moneti, G., Richich B., Nativi, C. (2010). Stable GM3 lactone mimetic raises antibodies specific for the antigens expressed on melanoma cells. Bioconj. Chem. 29(8):1432–1438.
   Google Scholar
• Beck, A., Hillen, N., Dolashki, A., Stevanovic, S., Salvato, B., Voelter, W., Dolashka-Angelova, P. (2007). Oligosaccharide structure of a functional unit RvH1-b of Rapana venosa hemocyanin using HPLC/electrospray ionization mass spectrometry. Biochimie 89(8):938–949.
   PubMedGoogle Scholar
• Benjamin, D. C., Berzofsky, J. A., East, I.J. (1984). The antigenic structure of proteins: a reappraisal. Annu. Rev. Immunol. 2:67–101.
   PubMed Web of Science ®Google Scholar
• Bonaventura, J., Bonaventura, C. (1980). Hemocyanins relationships in their structure, function and assembly. Amer. Zool., 20(1):7–17.
   Google Scholar
• Carr, S. A., Huddleston, M. J., Bean, M. F. (1993). Selective identification and differentiation of N- and O-linked oligosaccharides in glycoproteins by liquid chromatography-mass spectrometry. Protein Sci. 2:183–196.
   PubMed Web of Science ®Google Scholar
• Chiarella, P., Edelmann, B., Fazio, V. M., Sawyer, A. M., de Marco, A. (2010). Antigenic features of protein carriers commonly used in immunisation trials. Biotechnol. Lett. 32(9):1215–1221.
   Google Scholar
• Celluzzi, C. M., Mayordomo, I. J., Storkus, J. W., Lotze, T. M., Falo, D. L. (1996). Peptide-pulsed dendritic cells induce antigen-specific CTL-mediated protective tumor immunity. J. Exp. Med. 183:283–287.
   PubMed Web of Science ®Google Scholar
• Dolashka-Angelova, P., Beck, A.; Dolashki, A., Beltramini, M., Stevanovic, S., Salvato, B., Hristova, R., Velkova, L., Voelter, W. (2004). Carbohydrate moieties of molluscan Rapana venosa hemocyanin. Micron 35:101–104.
   PubMedGoogle Scholar
• Dolashka-Angelova, P., Lieb, B.; Velkova, L., Heilen, N., Sandra, K., Nikolaeva-Glomb, L., Dolashki, A., Galabov, A. S., Beeumen, J. V., Stevanovic, S., Voelter, W., Devreese, B. (2009). Identification of glycosylated sites in Rapana hemocyanin by mass spectrometry and gene sequence, and their antiviral effect. Bioconjug Chem. 20(7):1315–1322.
   PubMed Web of Science ®Google Scholar
• Dolashka-Angelova, P., Schwarz, H., Dolashki, A., Beltramini, M., Salvato, B., Schick, M., Saeed, M., Voelter, W. (2003). Oligomeric stability of Rapana venosa hemocyanin (RvH) and its structural subunits. Biochim. Biophys. Acta 1646(1–2):77–85.
   PubMedGoogle Scholar
• Dolashka-Angelova, P., Stefanova, T., Livaniou, E., Velkova, L., Klimentzou, P., Stevanovic, S., Neychev, H., Schwarz, H., Voelter, W. (2008). Immunological potential of Helix vulgaris and Rapana venosa hemocyanins. Immunol. Invest. 37(8): 822–40.
   PubMed Web of Science ®Google Scholar
• Donald, L., Jean, I., Dehaven, R., Riggs, D. (2000). Keyhole limpet hemocyanin immunotherapy of bladder cancer: Laboratory and clinical studies. Eur. Urol. (37):41–44.
   Google Scholar
• Gielens, C., De Geest, N., Compernolle, F., Préaux, G. (2004). Glycosylation sites of hemocyanins of Helix pomatia and Sepia officinalis. Micron 35:99–100.
   PubMedGoogle Scholar
• Harris, J. R., Markl, J. (1999). Keyhole limpet hemocyanin (KLH): A biomedical review. Micron 30(6):597–623.
   PubMed Web of Science ®Google Scholar
• Harris, R. J., Markl, J. (2000). Keyhole limpet hemocyanin: Molecular structure of a potent marine immunoactivator. Eur. Urol. 37:24–33.
   PubMed Web of Science ®Google Scholar
• Hartmann, H., Bongers, A., Decker, H. (2004). Small-angle X-ray scattering-based three-dimensional reconstruction of the immunogen KLH1 reveals different oxygen-dependent conformations. J. Biol. Chem. 279(4):2841–2845.
   Google Scholar
• Herscowitz, H. B., Harold, W. W., Stravitzky, B. A. (1972). Immunochemical and immunogenic properties of a purified keyhold limpet haemocyanin. Immunology 22:51–61.
   PubMed Web of Science ®Google Scholar
• Hewitt, J. (2009). Abnormal glycosylation of dystroglycan in human genetic disease. Review. Biochim. Biophys. Acta.
   Google Scholar
• Kafi, K., Betting, D. J., Yamada, R. E., Bacica, M., Steward, K. K., Timmerman, J. M. (2009). Maleimide conjugation markedly enhances the immunogenicity of both human and murine idiotype-KLH vaccines. Mol Immunol. 46(3):448–456.
   PubMed Web of Science ®Google Scholar
• Kirkin, A., Dzhandzhugazyan, K., Zeuthen, J. (1998). The immunogenic properties of melanoma-associated antigens recognized by cytotoxic T lymphocytes. Exp. Clin. Immunogen. 15(1):19–32.
   Google Scholar
• Kurokawa, T., Wuhrer, M., Lochnit, G., Geyer, H., Markl, J., Geyer, R. (2002). Hemocyanin from the keyhole limpet Megathura crenulata (KLH) carries a novel type of N-glycans with Gal(α1–6)Man-motifs. Eur. J. Biochem. 269:5459–5473.
   PubMedGoogle Scholar
• Laemmli U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685.
   PubMed Web of Science ®Google Scholar
• Lamping, N., Hoess, A., Yu, B., Park, T. C., Kirschning, C.J., Pfeil, D., Reuter, D., Wright, S. D., Herrmann, F., Schumann, R. R. (1996). Effects of site-directed mutagenesis of basic residues (Arg 94, Lys 95, Lys 99) of lipopolysaccharide (LPS)-binding protein on binding and transfer of LPS and subsequent immune cell activation. J. Immunol. 157(10):4648–4656.
   PubMed Web of Science ®Google Scholar
• Lommerse, J. P. M., Thomas-Oates, J. E., Gielens, C., Preaux, G., Kamerling, J. P., Vliegenthart, J. F. G. (1997). Primary structure of 21 novel monoantennary and diantennary N-linked carbohydrate chains from α-hemocyanin of Helix pomatia. Eur. J. Biochem. 249:195–222.
   PubMedGoogle Scholar
• Mailliard, R., Son, Y., Redlinger, R., Coates, P., Giermasz, A., Morel, P., Storkus, W., Kalinski, P. (2003). Dendritic cells mediate NK cell help for Th1 and CTL responses: Two-signal requirement for the induction of NK cell helper function. J. Immunol. 171:2366–2373.
   PubMed Web of Science ®Google Scholar
• Masson, P. R., Gwanzura, L. (1990). Reduced lymphocyte responses to mitogens in natural and experimental trichomoniasis. Infect. Immun. 58:3553–3557.
   Google Scholar
• Michele, D., Campbell, K. (2003). Dystrophin-glycoprotein complex: Post-translational processing and dystroglycan function. J. Biol. Chem. 278(18):15457–15460.
   Google Scholar
• Moltedo, B., Faunes, F., Haussmann, D., De Ioannes, P., De Ioannes, A., Puente, J., Becker, M. (2006). Immunotherapeutic effect of concholepas hemocyanin in the murine bladder cancer model: Evidence for conserved antitumor properties among hemocyanins. J. Urol. 176(6):2690–2695.
   PubMed Web of Science ®Google Scholar
• O'Brien-Simpson, N. M., Ede, N. J., Brown, L. E. (1997). Polymerization of unprotected synthetic peptides: A view toward synthetic peptide vaccines. J. Am. Chem. Soc. 119:1183–1188.
   Google Scholar
• Oyelaran, O., Gildersleeve, J. (2010). Evaluation of human antibody responses to keyhole limpet hemocyanin on a carbohydrate microarray. PROTEOMICS Clin. Appl. 4(3):285–294.
   Google Scholar
• Pearson, G. R. (1978). In vitro and in vivo investigations on antibody-dependent cellular cytotoxicity. Curr. Topics Microbiol. Immunol. 80:65–96.
   PubMedGoogle Scholar
• Pellis, N. R., Shulan, D. J., Kahan, B. D. (1976). Specific tumor immunity induced with soluble materials: Purification of antigens inducing tumor resistance. Biochem. Biophys. Res. Commun. 71:1251–1258.
   Google Scholar
• Plitnick, L. M., Herzyk, D. J. (2010). The T-dependent antibody response to keyhole limpet hemocyanin in rodents. Meth. Mol Biol. 598:159–171.
   PubMedGoogle Scholar
• Rabinovitch, P. S., June, C. H., Grossmann, A., Ledbetter, J. A. (1986). Heterogeneity among T cells in intracellular free calcium responses after mitogen stimulation with PHA or anti-CD3. Simultaneous use of indo-1 and immunofluorescence with flow cytometry. J. Immunol. 137(3):952–961.
   Google Scholar
• Salvato, B., Beltramini, M. (1990). Hemocyanins: molecular architecture, structure and reactivity of the binuclear copper active site. Life Chem. Rep. 8:1–47.
   Google Scholar
• Sandra, K., Dolashka-Angelova, P., Devreese, B., Van Beeumen, J. (2007). New insights in Rapana venosa hemocyani N-glycosylation resulting from on-line mass spectrometric analyses. Glycobiology 17(2):141–156.
   PubMedGoogle Scholar
• Schnurr, M., Galambus, P., Scholz, C., Then, F., Dauer, M., Endres, S., Eigler, A. (2001). Tumor cell lysate pulsed dendritic cells induce a T-cell response against pancreatic carcinoma cells: an in vitro model for tumor vaccines. Cancer Res. 61:6445–6450.
   PubMed Web of Science ®Google Scholar
• Schumacher, K. (2001). Keyhole limpet hemocyanin (KLH) conjugate vaccines as novel therapeutic tools in malignant disorders. J. Cancer Res. Clin. Oncol. 127(Suppl. 2): R1–R2.
   Google Scholar
• Schütz, J., Dolashka-Angelova, P., Abrashev, R., Nicolov, P., Voelter, W. (2001). Isolation and spectroscopic characterization of the structural subunits of keyhole limpet hemocyanin. Biochim. Biophys. Acta 1546:325–336.
   PubMedGoogle Scholar
• Teitz-Tennenbaum, S., Li, Q., Davis, M. A., Chang, A. E. (2008). Dendritic cells pulsed with keyhole limpet hemocyanin and cryopreserved maintain anti-tumor activity in a murine melanoma model.Clin. Immunol. 129(3):482–491.
   Google Scholar
• Terwilliger, N. B. (1998). Functional adaptations of oxygen-transport proteins. J. Exp. Biol. 201:1085–1098.
   PubMed Web of Science ®Google Scholar
• Timmerman, J. M., Levy, R. (2000). Linkage of foreign carrier protein to a self-tumor antigen enhances the immunogenicity of a pulsed dendritic cell vaccine. J. Immunol. 164(9):4797–4803.
   PubMed Web of Science ®Google Scholar
• Van Holde K., Miller, K., Decker, H. (2001). Hemocyanins and invertebrate evolution. J. Biol. Chem. 276:15563–15566.
   PubMed Web of Science ®Google Scholar
• Van Kuik, J. A., van Halbeek, H., Kamerling, J. P., Vliegenthart, J. F. (1985). Primary structure of the low-molecular-weight carbohydrate chains of Helix pomatia alpha-hemocyanin. Xylose as a constituent of N-linked oligosaccharides in an animal glycoprotein. J. Biol. Chem. 260(26):13984–13988.
   Google Scholar
• Velkova, L., Todorov, D., Dimitrov, I., Shishkov, S., Van Beeumen. J., Dolashka-Angelova, P. (2009). Rapana venosa hemocyanin with antiviral activity. Biotech. Biotech. Equip. 23(2):606–610.
   Google Scholar
• Wandall, H. H., Blixt, O., Tarp, M. A., Pedersen, J. W., Bennett, E. P., Mandel, U., Ragupathi, G., Livingston, P. O., Hollingsworth, M. A., Taylor-Papadimitriou, J., Burchell, J., Clausen, H. (2010). Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Res. 70(4):1306–1313.
   PubMed Web of Science ®Google Scholar
• Wirguin, I., Suturkova, M., Milosevic, L., Briani, C., Latov, N. (1995). Keyhole limpet hemocyanin contains Gal(β1-3)-GalNAc determinants that are cross-reactive with the T antigen. Cancer Immunol. 40:307–310.
   Google Scholar
• Wuhrer, M., Robijn, M. L. M., Koeleman, C. A. M., Balog, C. I. A., Geyer, R., Deelder, A. M., Hokke, C. H. (2004). A novel Gal(β1-4)Gal(β1-4)Fuc(α1-6)-core modification attached to the proximal N-acetylglucosamine of keyhole limpet hemocyanin (KLH) N-glycans. Biochem. J. 378:625–632.
   PubMed Web of Science ®Google Scholar
• Zhang, S., Graeber, L. A., Helling, F., Ragupathy, G., Adluri, S., Lioyd, K., Livingston, P. (1996). Cancer Res. 56:3315–3319.
   PubMed Web of Science ®Google Scholar