Anti-NeuGcGM3 antibodies, actively elicited by idiotypic vaccination in nonsmall cell lung cancer patients, induce tumor cell death by an oncosis-like mechanism

Journal of Immunology

Volumn 186, Issue 6, 2011, Pages 3735-3744

  Hernández, Ana María ^a   Rodríguez, Nely ^a   González, Jorge E ^b   Reyes, Emma ^c   Rondón, Teresa ^a   Griñán, Tania ^a   Macías, Amparo ^a   Alfonso, Sailyn ^d   Vázquez, Ana María ^a   Pérez, Rolando ^a  

^a CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

^b Center for Radiation Protection and Hygiene   (Cuba)

^c Criminality Central Laboratory   (Cuba)

^d Hospital Celestino Hernandez Robau   (Cuba)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GANGLIOSIDE ANTIBODY; NEUGCGM3 ANTIBODY; RACOTUMOMAB; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER PATIENT; CASE REPORT; CELL DEATH; CELL LOSS; CELL SWELLING; CHROMATIN CONDENSATION; DNA FRAGMENTATION; DRUG CYTOTOXICITY; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MULTIPLE CYCLE TREATMENT; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; TUMOR CELL; VACCINATION;

ANIMALS; ANTIBODIES, NEOPLASM; CANCER VACCINES; CARCINOMA, LEWIS LUNG; CARCINOMA, NON-SMALL-CELL LUNG; CELL DEATH; CELL LINE, TUMOR; DOGS; G(M3) GANGLIOSIDE; HORSES; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN IDIOTYPES; IMMUNOGLOBULIN M; LEUKEMIA L1210; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; PLASMACYTOMA;

EID: 79953180541     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000609     Document Type: Article

References (69)

1. Irie, A., S. Koyama, Y. Kozutsumi, T. Kawasaki, and A. Suzuki. 1998. The molecular basis for the absence of N-glycolylneuraminic acid in humans. J. Biol. Chem. 273: 15866-15871.
2. Irie, A., and A. Suzuki. 1998. CMP-N-Acetylneuraminic acid hydroxylase is exclusively inactive in humans. Biochem. Biophys. Res. Commun. 248: 330-333.
3. Olson, M. V., and A. Varki. 2003. Sequencing the chimpanzee genome: insights into human evolution and disease. Nat. Rev. Genet. 4: 20-28.
4. Malykh, Y. N., R. Schauer, and L. Shaw. 2001. N-Glycolylneuraminic acid in human tumours. Biochimie 83: 623-634. (Pubitemid 32821226)
5. Marquina, G., H. Waki, L. E. Fernández, K. Kon, A. Carr, O. Valiente, R. Pérez, and S. Ando. 1996. Gangliosides expressed in human breast cancer. Cancer Res. 56: 5165-5171. (Pubitemid 26383031)
6. Miyake, M., K. Hashimoto, M. Ito, O. Ogawa, E. Arai, S. Hitomi, and R. Kannagi. 1990. The abnormal occurrence and the differentiation-dependent distribution of N-acetyl and N-glycolyl species of the ganglioside GM2 in human germ cell tumors. A study with specific monoclonal antibodies. Cancer 65: 499-505. (Pubitemid 20058367)
7. Nguyen, D. H., P. Tangvoranuntakul, and A. Varki. 2005. Effects of natural human antibodies against a nonhuman sialic acid that metabolically incorporates into activated and malignant immune cells. J. Immunol. 175: 228-236. (Pubitemid 40884323)
8. Bardor, M., D. H. Nguyen, S. Diaz, and A. Varki. 2005. Mechanism of uptake and incorporation of the non-human sialic acid N-glycolylneuraminic acid into human cells. J. Biol. Chem. 280: 4228-4237.
9. Yin, J., A. Hashimoto, M. Izawa, K. Miyazaki, G. Y. Chen, H. Takematsu, Y. Kozutsumi, A. Suzuki, K. Furuhata, F. L. Cheng, et al. 2006. Hypoxic culture induces expression of sialin, a sialic acid transporter, and cancer-associated gangliosides containing non-human sialic acid on human cancer cells. Cancer Res. 66: 2937-2945.
10. Potapenko, M., G. V. Shurin, and J. de León. 2007. Gangliosides as immunomodulators. Adv. Exp. Med. Biol. 601: 195-203.
11. Roque-Navarro, L., K. Chakrabandhu, J. de León, S. Rodríguez, C. Toledo, A. Carr, C. M. de Acosta, A. O. Hueber, and R. Pérez. 2008. Anti-ganglioside antibody-induced tumor cell death by loss of membrane integrity. Mol. Cancer Ther. 7: 2033-2041.
12. Retter, M. W., J. C. Johnson, D. W. Peckham, J. E. Bannink, C. S. Bangur, K. Dresser, F. Cai, T. M. Foy, N. A. Fanger, G. R. Fanger, et al. 2005. Characterization of a proapoptotic antiganglioside GM2 monoclonal antibody and evaluation of its therapeutic effect on melanoma and small cell lung carcinoma xenografts. Cancer Res. 65: 6425-6434. (Pubitemid 40994431)
13. Aixinjueluo, W., K. Furukawa, Q. Zhang, K. Hamamura, N. Tokuda, S. Yoshida, R. Ueda, and K. Furukawa. 2005. Mechanisms for the apoptosis of small cell lung cancer cells induced by anti-GD2 monoclonal antibodies: roles of anoikis. J. Biol. Chem. 280: 29828-29836.
14. Alfonso, M., A. Díaz, A. M. Hernández, A. Pérez, E. Rodríguez, R. Bitton, R. Pérez, and A. M. Vázquez. 2002. An anti-idiotype vaccine elicits a specific response to N-glycolyl sialic acid residues of glycoconjugates in melanoma patients. J. Immunol. 168: 2523-2529.
15. Neninger, E., R. M. Díaz, A. de la Torre, R. Rives, A. Díaz, G. Saurez, M. R. Gabri, D. F. Alonso, B. Wilkinson, A. M. Alfonso, et al. 2007. Active immunotherapy with 1E10 anti-idiotype vaccine in patients with small cell lung cancer: report of a phase I trial. Cancer Biol. Ther. 6: 145-150.
16. Díaz, A., M. Alfonso, R. Alonso, G. Saurez, M. Troche, M. Catalá, R. M. Díaz, R. Pérez, and A. M. Vázquez. 2003. Immune responses in breast cancer patients immunized with an anti-idiotype antibody mimicking NeuGc-containing gangliosides. Clin. Immunol. 107: 80-89.
17. Hernández, A. M., D. Toledo, D. Martínez, T. Griñán, V. Brito, A. Macías, S. Alfonso, T. Rondón, E. Suárez, A. M. Vázquez, and R. Pérez. 2008. Characterization of the antibody response against NeuGcGM3 ganglioside elicited in non-small cell lung cancer patients immunized with an anti-idiotype antibody. J. Immunol. 181: 6625-6634.
18. Vázquez, A. M., A. Pérez, A. M. Hernández, A. Macías, M. Alfonso, G. Bombino, and R. Pérez. 1998. Syngeneic anti-idiotypic monoclonal antibodies to an anti-NeuGc-containing ganglioside monoclonal antibody. Hybridoma 17: 527-534. (Pubitemid 29024638)
19. Vázquez, A. M., M. Alfonso, B. Lanne, K. A. Karlsson, A. Carr, O. Barroso, L. E. Fernández, E. Rengifo, M. E. Lanio, C. Alvarez, et al. 1995. Generation of a murine monoclonal antibody specific for N-glycolylneuraminic acid-containing gangliosides that also recognizes sulfated glycolipids. Hybridoma 14: 551-556. (Pubitemid 26028517)
20. Moreno, E., B. Lanne, A. M. Vázquez, I. Kawashima, T. Tai, L. E. Fernández, K. A. Karlsson, J. Angström, and R. Pérez. 1998. Delineation of the epitope recognized by an antibody specific for N-glycolylneuraminic acid-containing gangliosides. Glycobiology 8: 695-705. (Pubitemid 28331445)
21. Alfonso, S, R. M. Diaz, A. de la Torre, E. Santiesteban, F. Aguirre, K. Pérez, and J. L. Rodríguez, M. del C. Barroso, A. M. Hernández, et al. 2007. 1E10 anti-idiotype vaccine in non-small cell lung cancer: experience in stage IIIb/IV patients. Cancer Biol. Ther. 6: 1847-1852.
22. Stults, C. L. M., C. C. Sweeley, and B. A. Macher. 1989. Glycosphingolipids: structure, biological source, and properties. Methods Enzymol. 179: 167-214.
23. Perea, S. E., O. Reyes, Y. Puchades, O. Mendoza, N. S. Vispo, I. Torrens, A. Santos, R. Silva, B. Acevedo, E. López, et al. 2004. Antitumor effect of a novel proapoptotic peptide that impairs the phosphorylation by the protein kinase 2 (casein kinase 2). Cancer Res. 64: 7127-7129. (Pubitemid 39331026)
24. Sestili, P., C. Martinelli, and V. Stocchi. 2006. The fast halo assay: an improved method to quantify genomic DNA strand breakage at the single-cell level. Mutat. Res. 607: 205-214.
25. Majno, G., and I. Joris. 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 146: 3-15.
26. Gichner, T., A. Mukherjee, E. D. Wagner, and M. J. Plewa. 2005. Evaluation of the nuclear DNA Diffusion Assay to detect apoptosis and necrosis. Mutat. Res. 586: 38-46.
27. Lecoeur, H., M. C. Prévost, and M. L. Gougeon. 2001. Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry 44: 65-72.
28. Denecker, G., H. Dooms, G. Van Loo, D. Vercammen, J. Grooten, W. Fiers, W. Declercq, and P. Vandenabeele. 2000. Phosphatidyl serine exposure during apoptosis precedes release of cytochrome c and decrease in mitochondrial transmembrane potential. FEBS Lett. 465: 47-52. (Pubitemid 30012113)
29. Sestili, P., F. Cattabeni, and O. Cantoni. 1996. Direct excision of 50 kb pair DNA fragments from megabase-sized fragments produced during apoptotic cleavage of genomic DNA. FEBS Lett. 396: 337-342. (Pubitemid 26377852)
30. Shi, Y. F., M. G. Szalay, L. Paskar, B. M. Sahai, M. Boyer, B. Singh, and D. R. Green. 1990. Activation-induced cell death in T cell hybridomas is due to apoptosis. Morphologic aspects and DNA fragmentation. J. Immunol. 144: 3326-3333.
31. Cohen, G. M., X. M. Sun, R. T. Snowden, D. Dinsdale, and D. N. Skilleter. 1992. Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochem. J. 286: 331-334.
32. Bacso, Z., and J. F. Eliason. 2001. Measurement of DNA damage associated with apoptosis by laser scanning cytometry. Cytometry 45: 180-186.
33. Gopalakrishna, P., and A. Khar. 1995. Comet assay to measure DNA damage in apoptotic cells. J. Biochem. Biophys. Methods 30: 69-73.
34. Jugdutt, B. I., and H. A. Idikio. 2005. Apoptosis and oncosis in acute coronary syndromes: assessment and implications. Mol. Cell. Biochem. 270: 177-200.
35. Palomba, L., P. Sestili, M. Columbaro, E. Falcieri, and O. Cantoni. 1999. Apoptosis and necrosis following exposure of U937 cells to increasing concentrations of hydrogen peroxide: the effect of the poly(ADP-ribose) polymerase inhibitor 3-aminobenzamide. Biochem. Pharmacol. 58: 1743-1750.
36. Matteucci, C., S. Grelli, E. De Smaele, C. Fontana, and A. Mastino. 1999. Identification of nuclei from apoptotic, necrotic, and viable lymphoid cells by using multiparameter flow cytometry. Cytometry 35: 145-153.
37. Shuji, M., A. Yoshihiro, S. Kunio, K. Hidehiro, Y. Iwao, Y. Hiroshi, U. Masanori, H. Katsuiku, and T. Tomio. 1995. A Novel Type of Cell Death of Lymphocytes Induced by a Monoclonal Antibody without Participation of Complement. J. Exp. Med. 181: 2007-2015.
38. Zhang, C., Y. Xu, J. Gu, and S. F. Schlossman. 1998. A cell surface receptor defined by a mAb mediates a unique type of cell death similar to oncosis. Proc. Natl. Acad. Sci. USA 95: 6290-6295.
39. Bhat, N. M., M. M. Bieber, F. K. Stevenson, and N. N. H. Teng. 1996. Rapid cytotoxicity of human B lymphocytes induced by VH4-34 (VH4.21) geneencoded monoclonal antibodies. Clin. Exp. Immunol. 105: 183-190.
40. Loo, D., N. Pryer, P. Young, T. Liang, S. Coberly, K. L. King, K. Kang, P. Roberts, M. Tsao, X. Xu, et al. 2007. The glycotope-specific RAV12 monoclonal antibody induces oncosis in vitro and has antitumor activity against gastrointestinal adenocarcinoma tumor xenografts in vivo. Mol. Cancer Ther. 6: 856-865.
41. Tan, H. L., W. J. Fong, E. H. Lee, M. Yap, and A. Choo. 2009. mAb 84, a cytotoxic antibody that kills undifferentiated human embryonic stem cells via oncosis. Stem Cells 27: 1792-1801.
42. Ma, F., C. Zhang, K. V. Prasad, G. J. Freeman, and S. F. Schlossman. 2001. Molecular cloning of Porimin, a novel cell surface receptor mediating oncotic cell death. Proc. Natl. Acad. Sci. USA 98: 9778-9783.
43. Zhu, A., and R. Hurst. 2002. Anti-N-glycolylneuraminic acid antibodies identified in healthy human serum. Xenotransplantation 9: 376-381. (Pubitemid 36358933)
44. Simons, M., T. Friedrichson, J. B. Schulz, M. Pitto, M. Masserini, and T. V. Kurzchalia. 1999. Exogenous administration of gangliosides displaces GPI-anchored proteins from lipid microdomains in living cells. Mol. Biol. Cell 10: 3187-3196.
45. Zitvogel, L., and G. Kroemer. 2008. The immune response against dying tumor cells: avoid disaster, achieve cure. Cell Death Differ. 15: 1-2. (Pubitemid 350286166)
46. Fonseca, C., and G. Dranoff. 2008. Capitalizing on the immunogenicity of dying tumor cells. Clin. Cancer Res. 14: 1603-1608.
47. Krysko, D. V., and P. Vandenabeele. 2008. From regulation of dying cell engulfment to development of anti-cancer therapy. Cell Death Differ. 15: 29-38. (Pubitemid 350286170)
48. Matzinger, P. 2007. Friendly and dangerous signals: is the tissue in control? Nat. Immunol. 8: 11-13. (Pubitemid 46242350)
49. Tesniere, A., T. Panaretakis, O. Kepp, L. Apetoh, F. Ghiringhelli, L. Zitvogel, and G. Kroemer. 2008. Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 15: 3-12. (Pubitemid 350286167)
50. Cerri, C., D. Chimenti, I. Conti, T. Neri, P. Paggiaro, and A. Celi. 2006. Monocyte/macrophage-derived microparticles up-regulate inflammatory mediator synthesis by human airway epithelial cells. J. Immunol. 177: 1975-1980. (Pubitemid 44092538)
51. Carp, H. 1982. Mitochondrial N-formylmethionyl proteins as chemoattractants for neutrophils. J. Exp. Med. 155: 264-275.
52. Czapiga, M., J. L. Gao, A. Kirk, and J. Lekstrom-Himes. 2005. Human platelets exhibit chemotaxis using functional N-formyl peptide receptors. Exp. Hematol. 33: 73-84.
53. Andersson, U., H. Wang, K. Palmblad, A. C. Aveberger, O. Bloom, H. Erlandsson-Harris, A. Janson, R. Kokkola, M. Zhang, H. Yang, and K. J. Tracey. 2000. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 192: 565-570.
54. Rouhiainen, A., J. Kuja-Panula, E. Wilkman, J. Pakkanen, J. Stenfors, R. K. Tuominen, M. Lepäntalo, O. Carpén, J. Parkkinen, and H. Rauvala. 2004. Regulationofmonocytemigration by amphoterin (HMGB1). Blood 104:1174-1182.
55. Collins, L. V., S. Hajizadeh, E. Holme, I. M. Jonsson, and A. Tarkowski. 2004. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J. Leukoc. Biol. 75: 995-1000.
56. Beutler, B., Z. Jiang, P. Georgel, K. Crozat, B. Croker, S. Rutschmann, X. Du, and K. Hoebe. 2006. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24: 353-389.
57. Fadok, V. A., D. L. Bratton, L. Guthrie, and P. M. Henson. 2001. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J. Immunol. 166: 6847-6854.
58. Brusa, D., E. Migliore, S. Garetto, M. Simone, and L. Matera. 2009. Immunogenicity of 56 degrees C and UVC-treated prostate cancer is associated with release of HSP70 and HMGB1 from necrotic cells. Prostate 69: 1343-1352.
59. Vanden Berghe, T., M. Kalai, G. Denecker, A. Meeus, X. Saelens, and P. Vandenabeele. 2006. Necrosis is associated with IL-6 production but apoptosis is not. Cell. Signal. 18: 328-335.
60. van der Most, R. G., A. J. Currie, B. W. Robinson, and R. A. Lake. 2008. Decoding dangerous death: how cytotoxic chemotherapy invokes inflammation, immunity or nothing at all. Cell Death Differ. 15: 13-20.
61. Ullrich, E., M. Bonmort, G. Mignot, G. Kroemer, and L. Zitvogel. 2008. Tumor stress, cell death and the ensuing immune response. Cell Death Differ. 15: 21-28. (Pubitemid 350286169)
62. Brusa, D., S. Garetto, G. Chiorino, M. Scatolini, E. Migliore, G. Camussi, and L. Matera. 2008. Post-apoptotic tumors are more palatable to dendritic cells and enhance their antigen cross-presentation activity. Vaccine 26: 6422-6432.
63. Shi, H., T. Cao, J. E. Connolly, L. Monnet, L. Bennett, S. Chapel, C. Bagnis, P. Mannoni, J. Davoust, A. K. Palucka, and J. Banchereau. 2006. Hyperthermia enhances CTL cross-priming. J. Immunol. 176: 2134-2141. (Pubitemid 43201660)
64. Todryk, S. M., J. Eaton, L. Birchall, R. Greenhalgh, D. Soars, A. G. Dalgleish, A. A. Melcher, and H. S. Pandha. 2004. Heated tumour cells of autologous and allogeneic origin elicit anti-tumour immunity. Cancer Immunol. Immunother. 53: 323-330.
65. Korbelik, M., J. Sun, and I. Cecic. 2005. Photodynamic therapy-induced cell surface expression and release of heat shock proteins: relevance for tumor response. Cancer Res. 65: 1018-1026. (Pubitemid 40216464)
66. Chen, T., J. Guo, C. Han, M. Yang, and X. Cao. 2009. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J. Immunol. 182: 1449-1459.
67. Davis, T. A., D. K. Czerwinski, and R. Levy. 1999. Therapy of B-cell lymphoma with anti-CD20 antibodies can result in the loss of CD20 antigen expression. Clin. Cancer Res. 5: 611-615.
68. Kowalczyk, A., M. Gil, I. Horwacik, Z. Odrowaz, D. Kozbor, and H. Rokita. 2009. The GD2-specific 14G2a monoclonal antibody induces apoptosis and enhances cytotoxicity of chemotherapeutic drugs in IMR-32 human neuroblastoma cells. Cancer Lett. 281: 171-182.
69. Pohle, T., S. Brändlein, N. Ruoff, H. K. Müller-Hermelink, and H. P. Vollmers. 2004. Lipoptosis: tumor-specific cell death by antibody-induced intracellular lipid accumulation. Cancer Res. 64: 3900-3906.