Targeting a novel onco-glycoprotein antigen at tumoral pancreatic cell surface by mAb16D10 induces cell death

Journal of Immunology

Volumn 189, Issue 7, 2012, Pages 3386-3396

  Crescence, Lydie ^a,b   Beraud, Evelyne ^a,b   Sbarra, Veronique ^a,b   Bernard, Jean Paul ^a,b,c   Lombardo, Dominique ^a,b,c   Mas, Eric ^a,b,c  

^a University of the Mediterranean Aix Marseille II   (France)

^b CNRS   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

16D10 ANTIGEN; BETA CATENIN; CASPASE; CYCLIN D1; GLYCOGEN SYNTHASE KINASE 3BETA; MEMBRANE ANTIGEN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 16D10; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; UNCLASSIFIED DRUG; UVOMORULIN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LIPID RAFT; PANCREAS CELL; PANCREAS TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; APOPTOSIS; CELL DEATH; CELL LINE, TUMOR; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, NUDE; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84866562769     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102647     Document Type: Article

References (57)

1. Jemal, A., R. Siegel, E. Ward, Y. Hao, J. Xu, T. Murray, and M. J. Thun. 2008. Cancer statistics, 2008. CA Cancer J. Clin. 58: 71-96. (Pubitemid 351521864)
2. Li, X., A. B. Roginsky, X. Z. Ding, C. Woodward, P. Collin, R. A. Newman, R. H. Bell, Jr., and T. E. Adrian. 2008. Review of the apoptosis pathways in pancreatic cancer and the anti-apoptotic effects of the novel sea cucumber compound, Frondoside A. Ann. N. Y. Acad. Sci. 1138: 181-198.
3. Hamacher, R., R. M. Schmid, D. Saur, and G. Schneider. 2008. Apoptotic pathways in pancreatic ductal adenocarcinoma. Mol. Cancer 7: 64.
4. Garcea, G., M. M. Manson, C. P. Neal, C. J. Pattenden, C. D. Sutton, A. R. Dennison, and D. P. Berry. 2007. Glycogen synthase kinase-3 beta; a new target in pancreatic cancer? Curr. Cancer Drug Targets 7: 209-215. (Pubitemid 46699072)
5. Giovannetti, E., V. Mey, S. Nannizzi, G. Pasqualetti, M. Del Tacca, and R. Danesi. 2006. Pharmacogenetics of anticancer drug sensitivity in pancreatic cancer. Mol. Cancer Ther. 5: 1387-1395. (Pubitemid 44070474)
6. Yip, Y. L., and R. L. Ward. 2002. Anti-ErbB-2 monoclonal antibodies and ErbB-2-directed vaccines. Cancer Immunol. Immunother. 50: 569-587.
7. Grillo-López, A. J., E. Hedrick, M. Rashford, and M. Benyunes. 2002. Rituximab: ongoing and future clinical development. Semin. Oncol. 29(1, Suppl 2)105-112. (Pubitemid 34173032)
8. Laheru, D., and E. M. Jaffee. 2005. Immunotherapy for pancreatic cancer - science driving clinical progress. Nat. Rev. Cancer 5: 459-467. (Pubitemid 40791488)
9. Durrant, L. G., S. J. Harding, N. H. Green, L. D. Buckberry, and T. Parsons. 2006. A new anticancer glycolipid monoclonal antibody, SC104, which directly induces tumor cell apoptosis. Cancer Res. 66: 5901-5909. (Pubitemid 43927145)
10. Gorter, A., and S. Meri. 1999. Immune evasion of tumor cells using membrane-bound complement regulatory proteins. Immunol. Today 20: 576-582.
11. Escribano, M. J., J. Cordier, M. Nap, F. J. Ten Kate, and P. Burtin. 1986. Differentiation antigens in fetal human pancreas. Reexpression in cancer. Int. J. Cancer 38: 155-160. (Pubitemid 16043589)
12. Escribano, M. J., and S. Imperial. 1989. Purification and molecular characterization of FAP, a feto-acinar protein associated with the differentiation of human pancreas. J. Biol. Chem. 264: 21865-21871. (Pubitemid 20028760)
13. Mas, E., N. Abouakil, S. Roudani, F. Miralles, O. Guy-Crotte, C. Figarella, M. J. Escribano, and D. Lombardo. 1993. Human fetoacinar pancreatic protein: an oncofetal glycoform of the normally secreted pancreatic bile-salt-dependent lipase. Biochem. J. 289: 609-615. (Pubitemid 23042078)
14. Lombardo, D. 2001. Bile salt-dependent lipase: its pathophysiological implications. Biochim. Biophys. Acta 1533: 1-28. (Pubitemid 32763262)
15. Aubert-Jousset, E., N. Garmy, V. Sbarra, J. Fantini, M. O. Sadoulet, and D. Lombardo. 2004. The combinatorial extension method reveals a sphingolipid binding domain on pancreatic bile salt-dependent lipase: role in secretion. Structure 12: 1437-1447. (Pubitemid 39092088)
16. Benkoël, L., J. P. Bernard, M. J. Payan-Defais, L. Crescence, C. Franceschi, M. Delmas, M. Ouaissi, B. Sastre, J. Sahel, A. M. Benoliel, et al. 2009. Monoclonal antibody 16D10 to the COOH-terminal domain of the feto-acinar pancreatic protein targets pancreatic neoplastic tissues. Mol. Cancer Ther. 8: 282-291.
17. Panicot-Dubois, L., M. Aubert, C. Franceschi, E. Mas, F. Silvy, C. Crotte, J. P. Bernard, D. Lombardo, and M. O. Sadoulet. 2004. Monoclonal antibody 16D10 to the C-terminal domain of the feto-acinar pancreatic protein binds to membrane of human pancreatic tumoral SOJ-6 cells and inhibits the growth of tumor xenografts. Neoplasia 6: 713-724. (Pubitemid 40041489)
18. Mas, E., E. Pasqualini, N. Caillol, A. El Battari, C. Crotte, D. Lombardo, and M. O. Sadoulet. 1998. Fucosyltransferase activities in human pancreatic tissue: comparative study between cancer tissues and established tumoral cell lines. Glycobiology 8: 605-613. (Pubitemid 28270582)
19. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63. (Pubitemid 14203433)
20. Ohnuma, K., T. Ishii, S. Iwata, O. Hosono, H. Kawasaki, M. Uchiyama, H. Tanaka, T. Yamochi, N. H. Dang, and C. Morimoto. 2002. G1/S cell cycle arrest provoked in human T cells by antibody to CD26. Immunology 107: 325-333. (Pubitemid 35356952)
21. Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408: 307-310.
22. Levine, A. J., W. Hu, and Z. Feng. 2006. The P53 pathway: what questions remain to be explored? Cell Death Differ. 13: 1027-1036.
23. Hermeking, H. 2007. p53 enters the microRNA world. Cancer Cell 12: 414-418. (Pubitemid 350046413)
24. Brady, C. A., D. Jiang, S. S. Mello, T. M. Johnson, L. A. Jarvis, M. M. Kozak, D. Kenzelmann Broz, S. Basak, E. J. Park, M. E. McLaughlin, et al. 2011. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 145: 571-583.
25. Dumont, P., J. I. Leu, A. C. Della Pietra, III, D. L. George, and M. Murphy. 2003. The codon 72 polymorphic variants of p53 have markedly different apoptotic potential. Nat. Genet. 33: 357-365. (Pubitemid 36278852)
26. Jeong, B. S., W. Hu, V. Belyi, R. Rabadan, and A. J. Levine. 2010. Differential levels of transcription of p53-regulated genes by the arginine/proline polymorphism: p53 with arginine at codon 72 favors apoptosis. FASEB J. 24: 1347-1353.
27. Miyashita, T., and J. C. Reed. 1995. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80: 293-299.
28. Hemann, M. T., and S. W. Lowe. 2006. The p53-Bcl-2 connection. Cell Death Differ. 13: 1256-1259. (Pubitemid 44057454)
29. Chen, X., and M. D. Resh. 2002. Cholesterol depletion from the plasma membrane triggers ligand-independent activation of the epidermal growth factor receptor. J. Biol. Chem. 277: 49631-49637. (Pubitemid 36014404)
30. Diehl, J. A., F. Zindy, and C. J. Sherr. 1997. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11: 957-972. (Pubitemid 27199876)
31. Inamoto, T., T. Yamochi, K. Ohnuma, S. Iwata, S. Kina, S. Inamoto, M. Tachibana, Y. Katsuoka, N. H. Dang, and C. Morimoto. 2006. Anti-CD26 monoclonal antibody-mediated G1-S arrest of human renal clear cell carcinoma Caki-2 is associated with retinoblastoma substrate dephosphorylation, cyclin-dependent kinase 2 reduction, p27(kip1) enhancement, and disruption of binding to the extracellular matrix. Clin. Cancer Res. 12: 3470-3477.
32. Kroemer, G., L. Galluzzi, P. Vandenabeele, J. Abrams, E. S. Alnemri, E. H. Baehrecke, M. V. Blagosklonny, W. S. El-Deiry, P. Golstein, D. R. Green, et al; Nomenclature Committee on Cell Death 2009. 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16: 3-11.
33. Chipuk, J. E., T. Kuwana, L. Bouchier-Hayes, N. M. Droin, D. D. Newmeyer, M. Schuler, and D. R. Green. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014. (Pubitemid 38209704)
34. Bryant, H. E., N. Schultz, H. D. Thomas, K. M. Parker, D. Flower, E. Lopez, S. Kyle, M. Meuth, N. J. Curtin, and T. Helleday. 2005. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434: 913-917. (Pubitemid 40559005)
35. Cañadillas, J. M., H. Tidow, S. M. Freund, T. J. Rutherford, H. C. Ang, and A. R. Fersht. 2006. Solution structure of p53 core domain: structural basis for its instability. Proc. Natl. Acad. Sci. USA 103: 2109-2114. (Pubitemid 43271631)
36. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825. (Pubitemid 23346378)
37. Diehl, J. A., M. Cheng, M. F. Roussel, and C. J. Sherr. 1998. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12: 3499-3511. (Pubitemid 28553242)
38. Takahashi-Yanaga, F., and T. Sasaguri. 2008. GSK-3beta regulates cyclin D1 expression: a new target for chemotherapy. Cell. Signal. 20: 581-589. (Pubitemid 351241128)
39. Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16: 3797-3804.
40. Liu, C., Y. Li, M. Semenov, C. Han, G. H. Baeg, Y. Tan, Z. Zhang, X. Lin, and X. He. 2002. Control of beta-catenin phosphorylation/degradation by a dualkinase mechanism. Cell 108: 837-847. (Pubitemid 34327534)
41. Kulikov, R., K. A. Boehme, and C. Blattner. 2005. Glycogen synthase kinase 3-dependent phosphorylation of Mdm2 regulates p53 abundance. Mol. Cell. Biol. 25: 7170-7180. (Pubitemid 41105913)
42. Watcharasit, P., G. N. Bijur, L. Song, J. Zhu, X. Chen, and R. S. Jope. 2003. Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J. Biol. Chem. 278: 48872-48879.
43. Lickert, H., A. Bauer, R. Kemler, and J. Stappert. 2000. Casein kinase II phosphorylation of E-cadherin increases E-cadherin/beta-catenin interaction and strengthens cell-cell adhesion. J. Biol. Chem. 275: 5090-5095. (Pubitemid 30108909)
44. Orford, K., C. Crockett, J. P. Jensen, A. M. Weissman, and S. W. Byers. 1997. Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J. Biol. Chem. 272: 24735-24738. (Pubitemid 27415637)
45. Wong, A. S., and B. M. Gumbiner. 2003. Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin. J. Cell Biol. 161: 1191-1203. (Pubitemid 36870179)
46. Chen, H. C., R. Y. Chu, P. N. Hsu, P. I. Hsu, J. Y. Lu, K. H. Lai, H. H. Tseng, N. H. Chou, M. S. Huang, C. J. Tseng, and M. Hsiao. 2003. Loss of E-cadherin expression correlates with poor differentiation and invasion into adjacent organs in gastric adenocarcinomas. Cancer Lett. 201: 97-106. (Pubitemid 37298002)
47. Li, Y. J., and X. R. Ji. 2003. Relationship between expression of E-cadherin-catenin complex and clinicopathologic characteristics of pancreatic cancer. World J. Gastroenterol. 9: 368-372.
48. Mǎ;rgineanu, E., C. E. Cotrutz, and C. Cotrutz. 2008. Correlation between E-cadherin abnormal expressions in different types of cancer and the process of metastasis. Rev. Med. Chir. Soc. Med. Nat. Iasi 112: 432-436.
49. Molina-Ortiz, I., R. A. Bartolomé, P. Hernández-Varas, G. P. Colo, and J. Teixidó. 2009. Overexpression of E-cadherin on melanoma cells inhibits chemokine-promoted invasion involving p190RhoGAP/p120ctn- dependent inactivation of RhoA. J. Biol. Chem. 284: 15147-15157.
50. Leong, K. G., K. Niessen, I. Kulic, A. Raouf, C. Eaves, I. Pollet, and A. Karsan. 2007. Jagged1-mediated Notch activation induces epithelial-to- mesenchymal transition through Slug-induced repression of E-cadherin. J. Exp. Med. 204: 2935-2948. (Pubitemid 350179562)
51. Oliveras-Ferraros, C., A. Vazquez-Martin, S. Cufí, B. Queralt, L. Báez, R. Guardeño, X. Hernández-Yagüe, B. Martin-Castillo, J. Brunet, and J. A. Menendez. 2011. Stem cell property epithelial-to-mesenchymal transition is a core transcriptional network for predicting cetuximab (Erbitux™) efficacy in KRAS wild-type tumor cells. J. Cell. Biochem. 112: 10-29.
52. Tettamanti, G., R. Bassi, P. Viani, and L. Riboni. 2003. Salvage pathways in glycosphingolipid metabolism. Biochimie 85: 423-437. (Pubitemid 36626013)
53. Lefrancois, S., T. May, C. Knight, D. Bourbeau, and C. R. Morales. 2002. The lysosomal transport of prosaposin requires the conditional interaction of its highly conserved d domain with sphingomyelin. J. Biol. Chem. 277: 17188-17199. (Pubitemid 34967752)
54. Sottocornola, E., R. Misasi, V. Mattei, L. Ciarlo, R. Gradini, T. Garofalo, B. Berra, I. Colombo, and M. Sorice. 2006. Role of gangliosides in the association of ErbB2 with lipid rafts in mammary epithelial HC11 cells. FEBS J. 273: 1821-1830. (Pubitemid 43779833)
55. Roitbak, T., Z. Surviladze, R. Tikkanen, and A. Wandinger-Ness. 2005. A polycystin multiprotein complex constitutes a cholesterol-containing signalling microdomain in human kidney epithelia. Biochem. J. 392: 29-38. (Pubitemid 41689398)
56. Deans, J. P., H. Li, and M. J. Polyak. 2002. CD20-mediated apoptosis: signalling through lipid rafts. Immunology 107: 176-182. (Pubitemid 35279043)
57. Patra, S. K. 2008. Dissecting lipid raft facilitated cell signaling pathways in cancer. Biochim. Biophys. Acta 1785: 182-206.