Immunodominant role of CCHA subunit of Concholepas hemocyanin is associated with unique biochemical properties

International Immunopharmacology

Volumn 9, Issue 3, 2009, Pages 330-339

  Becker, María Inés ^a,b   Fuentes, Alejandra ^a   Del Campo, Miguel ^a   Manubens, Augusto ^b   Nova, Esteban ^a   Oliva, Harold ^a   Faunes, Fernando ^a   Valenzuela, María Antonieta ^c   Campos Vallette, Marcelo ^c   Aliaga, Alvaro ^c   Ferreira, Jorge ^d   De Ioannes, Alfredo E ^b   De Ioannes, Pablo ^a   Moltedo, Bruno ^a  

^a Fundacion Ciencia y Tecnologia para el Desarrollo   (Chile)

^b Biosonda Corporation ^*  (Chile)

^c UNIVERSITY OF CHILE   (Chile)

^d UNIVERSITY OF CHILE   (Chile)

Author keywords

Bladder cancer; CCHA and CCHB subunits characterization; Concholepas concholepas; Hemocyanin; Immunogen; Immunotherapy

Indexed keywords

CARBOHYDRATE; CONCHOLEPAS CONCHOLEPAS HEMOCYANIN; CONCHOLEPAS CONCHOLEPAS HEMOCYANIN A; CONCHOLEPAS CONCHOLEPAS HEMOCYANIN B; HEMOCYANIN; SUGAR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOCHEMISTRY; BLADDER CANCER; BLADDER CARCINOMA; CANCER IMMUNIZATION; CANCER IMMUNOLOGY; CARBOHYDRATE ANALYSIS; CARCINOMA CELL; CHROMATOGRAPHY; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS REACTION; ELECTROPHORESIS; FEMALE; HUMORAL IMMUNITY; HYDROPHILICITY; IMMUNOCHEMISTRY; IMMUNOGENICITY; IMMUNOTHERAPY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPECTROSCOPY;

ANIMALS; ANTIBODY FORMATION; ANTINEOPLASTIC AGENTS; CARCINOMA; CELL LINE, TUMOR; CROSS REACTIONS; GASTROPODA; HEMOCYANIN; IMMUNOTHERAPY; KAPLAN-MEIERS ESTIMATE; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; PROTEIN SUBUNITS; URINARY BLADDER NEOPLASMS;

EID: 60249102375     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2008.12.011     Document Type: Article

References (63)

1. van Holde K.E., and Miller K.I. Hemocyanins. Adv Protein Chem 25 (1995) 1-8
2. van Holde K.E., Miller K.I., and Decker H. Hemocyanins and invertebrate evolution. J Biol Chem 276 (2001) 15563-15566
3. Mellema J.E., and Klug A. Quaternary structure of gastropod haemocyanin. Nature 239 (1972) 146-151
4. Orlova E.V., Dube P., Harris J.R., Beckman E., Zemlin F., Markl J., et al. Structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 Å resolution by electron cryomicroscopy and angular reconstitution. J Mol Biol 271 (1997) 417-437
5. Gebauer W., Harris J.R., Heid H., Üling S.M., Hillenbrand R., Söhngen S., et al. Quaternary structure, subunits and domain patterns of two discrete forms of keyhole limpet hemocyanin: KLH1 and KLH2. Zoology 98 (1994) 51-58
6. De Ioannes P., Moltedo B., Oliva H., Pacheco R., Faunes F., De Ioannes A.E., et al. Hemocyanin of the molluskan Concholepas concholepas exhibits an unusual heterodecameric array of subunits. J Biol Chem 279 (2004) 26134-26142
7. Weigle W.O. Immunochemical properties of hemocyanin. Immunochemistry 1 (1964) 295-26102
8. Harris J.R., and Markl K. Keyhole limpet hemocyanin (KLH): a biomedical review. Micron 30 (1999) 597-23
9. Musselli C., Livingstone P.O., and Rapugathi G.J. Keyhole limpet hemocyanin conjugate vaccine against cancer: the memorial Sloan Kettering experience. J Cancer Res Clin Oncol 127 Suppl 2 (2001) R20-R26
10. Kagan R., Rapupathi G., Yi S.S., Reis C.A., Gildersleeve J., Kahne D., et al. Comparison of antigen constructs and carrier molecules for augmenting the immunogenicity of the monosaccharide epithelial cancer antigen Tn. Cancer Immunol Immunother 54 (2005) 424-430
11. Sorensen A.L., Reis C.A., Tarp M.A., Mandel U., Ramachandran K., Sankaranarayanan V., et al. Chemoenzymatically synthesized multimeric Tn/STn MUC1 glycopeptides elicit cancer-specific anti-MUC1 antibody responses and override tolerance. Glycobiology 16 (2006) 96-07
12. Gatza E., and Okada C.Y. Tumor cell lysate-pulsed dendritic cells are more effective than TCR Id protein vaccines for active immunotherapy of T Cell Lymphoma. J Immunol 169 (2002) 5227-5235
13. Timmerman J.M., and Levy R. Linkage of foreign carrier protein to a self-tumor antigen enhances the immunogenicity of a pulsed dendritic cell. J Immuno1 64 (2000) 4797-03
14. Benchereau J., Ueno H., Dhodapkar M., Connolly J., Finholt J.P., Klechevsky E., et al. Immune and clinical outcomes in patients with stage IV melanoma vaccinated with peptide-pulsed dendritic cells derived from CD34+ progenitors and activated with type I interferon. J Immunother 28 (2005) 505-516
15. Escobar A., López M., Serrano A., Ramírez M., Pérez C., Aguirre A., et al. Dendritic cell immunization alone or combined with low doses of interleukin-2 induce specific immune responses in melanoma patients. Clin Exp Immunol 142 (2005) 555-568
16. Redman B.G., Chang A.E., Whitfield J., Esper P., Jiang G., Braun T., et al. Phase Ib trial assessing autologous, tumor-pulsed dendritic cells as a vaccine administered with or without IL-2 in patients with metastatic melanoma. J Immunother 31 (2008) 591-598
17. Jurincic-Winkler C.D., Metz K.A., Beuth J., and Klippel K.F. Keyhole limpet hemocyanin for carcinoma in situ of the bladder: a long-term follow-up study. Eur Urol 37 (2000) 45-49
18. Lamm D.L., Dehaven J.I., and Riggs D.R. Keyhole limpet hemocyanin immunotherapy of bladder cancer: laboratory and clinical studies. Eur Urol 37 Suppl. 3 (2000) 41-44
19. Gathuru J.K., Koide F., Rapupathi G.J., Adams L., Kerns R.T., Coleman T.P., et al. Identification of DHBcAg as a potent carrier protein comparable to KLH for augmenting MUC1 antigenicity. Vaccine 23 (2005) 4727-4733
20. Oliva H., Moltedo B., De Ioannes P., Faunes F., De Ioannes A.E., and Becker M.I. Monoclonal antibodies to molluskan hemocyanin from Concholepas concholepas demonstrate common and specific epitopes among subunits. Hybrid Hybridomics 21 (2002) 365-374
21. Swerdlow R.D., Ratliff T.L., La Regina M., Ritchey J.K., and Ebert R.F. Immunotherapy with keyhole limpet hemocyanin: Efficacy and safety in the MB-49 intravesical murine bladder tumor model. J Urol 151 (1994) 1718-1722
22. Leyton P, Lizama-Vergara PA, Campos-Vallette MM, Becker MI, Clavijo E, Córdova-Reyes IC et al. Surface enhanced Raman spectrum of nanometric molecular systems. J Chil Chem Soc 1005;50:725-30.
23. Duvillie B., Attali M., Aiello V., Quemeneur E., and Scharfmann R. Label-retaining cells in the rat pancreas. Location and differentiation potential in vitro. Diabetes 52 (2003) 2035-2042
24. Manosalva H., De Ioannes A.E., and Becker M.I. Development of monoclonal antibodies bearing the internal image of the gizzerosine epitope an application in a competitive ELISA for fish meal. Hybrid Hybridomics 23 (2004) 45-4
25. Cancino J., Torrealba C., Soza A., Yuseff M.I., Gravotta D., Henklein P., et al. Antibody to AP1B adaptor blocks biosynthetic and recycling routes of basolateral proteins at recycling endosomes. Mol Biol Cell 18 (2007) 4872-4884
26. Matus S., Burgos P.V., Bravo-Zehnder M., Kraft R., Porras O.H., Kraft O.H., Farías P., et al. Antiribosomal-P autoantibodies from psychiatric lupus target a novel neuronal surface protein causing calcium influx and apoptosis. J Exp Med 204 (2007) 3221-3234
27. Miller L.A., Talwar G.P., and Killian G.J. Contraceptive effect of a recombinant GnRH vaccine in adult female pigs. In: Timm R.M., and O'Brien J.M. (Eds). Proc. 22nd Vertebr. Pest. Conf (2006), Published at Univ. of Calif, Davis 106-109
28. Pilon J., Loiacono C., Okeson D., Lund S., Vercauteren K., Rhyan J., et al. Anti-prion activity generated by a novel vaccine formulation. Neurosci Lett 429 (2007) 161-164
29. Becker M.I., De Ioannes A.E., León C., and Ebensperguer L. Females of the communally breeding rodent, Octodon degus, transfer antibodies to their offspring during pregnancy and lactation. J Reprod Immunol 74 (2007) 68-7
30. Moltedo B., Faunes F., Haussmann D., De Ioannes P., De Ioannes A.E., Puente J., et al. Immunotherapeutic effect of Concholepas hemocyanin in the murine bladder cancer model: evidence for conserved antitumor properties among hemocyanins. J Urol 176 (2006) 2690-2695
31. Bradford M.M. A rapid and sensitive for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
32. De Ioannes P., Peirano A., Steiner J., and Eyzaguirre J. An alpha-l-arabinofuranosidase from Penicillium purpurogenum: production, purification and properties. J Biotechnology 76 (2000) 253-258
33. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
34. Morrisey J.H. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem 117 (1981) 307-310
35. Valenzuela M.A., Gamarra N., Gómez L., Kettlun A.M., Sardon M., Pérez L.M., et al. A comparative study of fish species identification by isoelectrofocusing, two-dimensional gel electrophoresis, and capillary zone electrophoresis. J Cap Electrophor Microchip Technol 6 (1999) 85-91
36. Walker J.M. Two-dimensional immunoelectrophoresis. In: Walker J.M. (Ed). The Protein Protocols Handbook (1996), Humana Press Inc, Totowa, New Jersey, USA 763-768
37. Keller H., Lieb B., Altenhein B., Gebauer D., Richter S., Stricker S., et al. Abalone (Haliotis tuberculata) hemocyanin type (HtH1). Organization of the approximately 400 kDa subunit, and amino acid sequence of its functional units f, g and h. Eur J Biochem 264 (1999) 27-28
38. Towbin H.E., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76 (1979) 4350-4354
39. Hounsell E.F., Davies M.J., and Smith K.D. Chemical methods of analysis of glycoproteins. In: Walker J.M. (Ed). The Protein Protocols Handbook (1996), Humana Press Inc, Totowa, New Jersey, USA 633-637
40. Hermanson G.T. Bioconjugate techniques (1996), Academic Press Inc, USA
41. Spiro R., and Bhoyroo V. Structure of the O-glycosidically linked carbohydrate units of fetuin. J Biol Chem 249 (1974) 5704-5717
42. Savage D., Mattson G., Desai S., Nielander G., Morgensen S., and Conklin E. Avidin-biotin chemistry: a handbook (1992), Pierce Chemical Company, Rockford IL, USA
43. Crowther J., and Abu-Elzeein E. Detection of antibodies against foot-and-mouth disease virus using purified Staphylococcus A protein conjugated with alkaline phosphatase. J Immunol Methods 34 (1980) 261-267
44. Wormald M.R., and Dwek R. Glycoproteins: glycan presentation and protein-fold stability. Structure 7 (1999) R155-R160
45. Linn JF, Black P, Derksen K, Rübben H, Thüroff JW. Keyhole limpet haemocyanin in experimental bladder cancer. Literature review and own results. Eur Urol 200;37(suppl 3):34-40.
46. Cerottini J.C., and Unanue E.R. Genetic control of the immune response of mice to hemocyanin. I. The role of macrophages. J Immunol 106 (1971) 732-739
47. Pavan Kumar G.V., Ashok A., Reddy M., Arif T., Kundu K., and Narayana C. Surface-enhanced Raman scattering studies of human transcriptional coactivator p300. J Phys Chem 110 (2006) 16787-16792
48. Cuff M.E., Miller K.I., van Holde K.E., and Hendrickson W.A. Crystal structure of a functional unit from Octopus hemocyanin. J Mol Biol 278 (1998) 855-870
49. Mouche F., Zhu Y., Pulokas J., Potter C.S., and Carragher B. Automated three-dimensional reconstruction of keyhole limpet hemocyanin type 1. J Struc Biol 144 (2003) 301-312
50. 4-macrocyclic metal complexes (2003), Springer, New York 725-790
51. Idakieva K., Nikolov P., Chakarska I., Genov N., and Shnyrov V.L. Spectroscopic properties and conformational stability of Concholepas concholepas hemocyanin. J Fluoresc 18 (2008) 715-725
52. Hopp T.P., and Woods K.R. Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci U S A 78 (1981) 3824-3828
53. Lanzavecchia A. Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annu Rev Immunol 8 (1990) 773-793
54. Jurincic-Winkler C.K., Metz A., Beuth J., Engelman U., and Klippel K.F. Immunohistological findings in patients with superficial bladder carcinoma after intravesical instillation of keyhole limpet haemocyanin. Br J Urol 76 (1995) 702-
55. Qi H., Egen J.G., Huang A.Y.C., and Germain R.N. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 312 (2006) 1672-1676
56. Siddiqui N.I., Idakieva K., Demarsin B., Doumanova L., Compernolle F., and Gielens C. Involvement of glycan chains in the antigenicity of Rapana thomasiana hemocyanin. Biochem Biophys Res Comm 361 (2007) 705-711
57. Kurokawa T., Wuhrer M., Lochnit G., Geyer H., Markl J., and Geyer R. Hemocyanin from the keyhole limpet Megathura crenulata (KLH) carries a novel type of N-glycans with Gal(β1-6)man-motifs. Eur J Biochem 269 (2002) 5459-5473
58. Paccagnella M., Bologna L., Beccaro M., Micetic I., Di Muro P., and Salvato B. Structural subunit organization of molluscan hemocyanins. Micron 35 (2004) 21-22
59. Presicce P., Taddeo A., Conti A., Villa M.L., and Bella S.D. Keyhole limpet hemocyanin induces the activation and maturation of human dendritic cells through the involvement of mannose receptor. Mol Immunol 45 (2008) 1136-1145
60. Stoeva S., Schütz J., Gebauer W., Hundsdörfer T., Manz C., Markl J., et al. Primary structure and unusual carbohydrate moiety of functional unit 2-c of keyhole limpet hemocyanin (KLH). Biochim Biophys Acta 1435 (1999) 94-09
61. Wirguin I., Suturkova-Milosevic L., Briani C., and Latov N. Keyhole-limpet hemocyanin contains Gal(beta 1-3)-GalNac determinants that are cross-reactive with the T antigen. Cancer Immunol Immunother 40 (1995) 307-310
62. Swerdlow R.D., Ebert R.F., Bonaventura C., and Miller K.I. KLH: structural and functional characterization of two different subunits and multimers. Comp Biochem Physiol B Biochem Mol Biol 113 (1996) 537-548
63. Tchorbanov A., Idakieva K., Mihaylova N., and Doumanova L. Modulation of the immune response using Rapana thomasiana hemocyanin. Intern Immunopharmacol 8 (2008) 1033-1038