Mucin-like peptides from Echinococcus granulosus induce antitumor activity

International Journal of Oncology

Volumn 43, Issue 3, 2013, Pages 775-784

  Noya, Verónica ^a   Bay, Sylvie ^b,c   Festari, María Florencia ^a,d   García, Enrique P ^a   Rodriguez, Ernesto ^a   Chiale, Carolina ^a   Ganneau, Christelle ^b,c   Baleux, Françoise ^b,c   Astrada, Soledad ^e   Bollati Fogolín, Mariela ^e   Osinaga, Eduardo ^a,d   Freire, Teresa ^a,d  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^b INSTITUT PASTEUR   (France)

^c CNRS   (France)

^d Laboratory of Tumor Glycobiology and Immunology   (France)

^e INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

Author keywords

Cancer; Dendritic cell; Echinococcus granulosus; Immunotherapy; Mucin; NK cell; Peptide

Indexed keywords

ANTINEOPLASTIC AGENT; CD69 ANTIGEN; ECHINOCOCCUS GRANULOSUS MUCIN LIKE PEPTIDE; HELMINTH PROTEIN; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TUMOR VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELL ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; ECHINOCOCCUS GRANULOSUS; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TUMOR CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ANTINEOPLASTIC AGENTS; CANCER VACCINES; DENDRITIC CELLS; ECHINOCOCCUS GRANULOSUS; HUMANS; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-6; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; MICE; MUCINS; NEOPLASMS; PEPTIDES; SPLEEN;

EID: 84880637362     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.2000     Document Type: Article

References (52)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127: 2893-2917, 2010.
2. de Martel C, Ferlay J, Franceschi S, et al: Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13: 607-615, 2012.
3. Benamrouz S, Conseil V, Creusy C, Calderon E, Dei-Cas E and Certad G: Parasites and malignancies, a review, with emphasis on digestive cancer induced by Cryptosporidium parvum (Alveolata: Apicomplexa). Parasite 19: 101-115, 2012.
4. Oliveira EC, Leite MS, Miranda JA, et al: Chronic Trypanosoma cruzi infection associated with low incidence of 1,2-dimethylhydrazine-induced colon cancer in rats. Carcinogenesis 22: 737-740, 2001.
5. Chen L, He Z, Qin L, et al: Antitumor effect of malaria parasite infection in a murine Lewis lung cancer model through induction of innate and adaptive immunity. PLoS One 6: e24407, 2011.
6. Wang XL, Fu BQ, Yang SJ, et al: Trichinella spiralis - a potential antitumor agent. Vet Parasitol 159: 249-252, 2009.
7. Akgül H, Tez M, Unal AE, Keşkek M, Sayek I and Ozçelik T: Echinococcus against cancer: why not? Cancer Immunol Immunother 98: 1999-2000, 2003.
8. Darani HY and Yousefi M: Parasites and cancers: parasite antigens as possible targets for cancer immunotherapy. Future Oncol 8: 1529-1235, 2012.
9. Yousofi Darani H, Soozangar N, Khorami S, Taji F, Yousofi M and Shirzad H: Hydatid cyst protoscolices induce cell death in WEHI-164 fibrosarcoma cells and inhibit the proliferation of baby hamster kidney fibroblasts in vitro. J Parasitol Res 304183: January 31, 2012. doi: 10.1155/2012/304183.
10. Medzhitov R: Recognition of microorganisms and activation of the immune response. Nature 449: 819-826, 2007.
11. Palucka AK, Ueno H, Fay JW and Banchereau J: Taming cancer by inducing immunity via dendritic cells. Immunol Rev 220: 129-150, 2007.
12. Correale J and Farez M: Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms. J Immunol 183: 5999-6012, 2009.
13. Elliott DE and Weinstock JV: Helminth-host immunological interactions: prevention and control of immune-mediated diseases. Ann NY Acad Sci 1247: 83-96, 2012.
14. van Vliet, SJ, van Liempt E, Saeland E, et al: Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int Immunol 17: 661-669, 2005.
15. Vanhoutte F, Breuilh L, Fontaine J, et al: Toll-like receptor (TLR)2 and TLR3 sensing is required for dendritic cell activation, but dispensable to control Schistosoma mansoni infection and pathology. Microbes Infect 9: 1606-1613, 2007.
16. Cummings RD and Nyame AK: Schistosome glysoconjugates. Biochim Biophys Acta 1455: 363-374, 1999.
17. Doedens A, Loukas A and Maizels RM: A cDNA encoding Tc-MUC-5, a mucin from Toxocara canis larvae identified by expression screening. Acta Trop 79: 211-217, 2001.
18. Theodoropoulos G, Hicks SJ, Corfield AP, Miller BG and Carrington SD: The role of mucins in host-parasite interactions: Part II - helminth parasites. Trends Parasitol 17: 130-135, 2001.
19. Thomas PG and Harn DAJ: Immune biasing by helminth glycans. Cell Microbiol 6: 13-22, 2004.
20. Alvarez Errico D, Medeiros A, Míguez M, et al: O-glycosylation in Echinococcus granulosus: identification and characterization of the carcinoma-associated Tn antigen. Exp Parasitol 98: 100-109, 2001.
21. Brockhausen I: Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep 7: 599-604, 2006.
22. Schietinger A, Philip M, Yoshida BA, Azadi P, Liu H, Meredith SC and Schreiber H: A mutant chaperone converts a wild-type protein into a tumor-specific antigen. Science 314: 304-308, 2006.
23. Baldus SE, Engelmann K and Hanisch FG: MUC1 and the MUCs: a family of human mucins with impact in cancer biology. Crit Rev Clin Lab Sci 41: 189-231, 2004.
24. Carraway KL III, Funes M, Workman HC and Sweeney C: Contribution of membrane mucins to tumor progression through modulation of cellular growth signaling pathways. Curr Top Dev Biol 78: 1-22, 2007.
25. Freire T and Osinaga E: The sweet side of tumor immunotherapy. Immunotherapy 4: 719-734, 2012.
26. Kufe DW: Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 9: 874-885, 2009.
27. Beatson RE, Taylor-Papadimitriou J and Burchell JM: MUC1 immunotherapy. Immunotherapy 2: 305-327, 2010.
28. Quoix E, Ramlau R, Westeel V, et al: Therapeutic vaccination with TG4010 and first-line chemotherapy in advanced non-small-cell lung cancer: a controlled phase 2B trial. Lancet Oncol 12: 1125-1133, 2011.
29. Slovin SF, Ragupathi G, Musselli C, et al: Fully synthetic carbohydrate-based vaccines in biochemically relapsed prostate cancer: clinical trial results with alpha-N-acetylgalactosamine-O-serine/threonine conjugate vaccine. J Clin Oncol 21: 4292-4298, 2003.
30. Fernandez C, Gregory WF, Loke P and Maizels RM: Full-length-enriched cDNA libraries from Echinococcus granulosus contain separate populations of oligo-capped and trans-spliced transcripts and a high level of predicted signal peptide sequences. Mol Biochem Parasitol 122: 171-180, 2002.
31. Coïc YM, Lan CL, Neumann JM, Jamin N and Baleux F: Slightly modifying pseudoproline dipeptides incorporation strategy enables solid phase synthesis of a 54 AA fragment of caveolin-1 encompassing the intramembrane domain. J Pept Sci 16: 98-104, 2010.
32. Lo-Man R, Vichier-Guerre S, Perraut R, et al: A fully synthetic therapeutic vaccine candidate targeting carcinoma-associated Tn carbohydrate antigen induces tumor-specific antibodies in nonhuman primates. Cancer Res 64: 4987-4994, 2004.
33. Rosa DS, Ribeiro SP and Cunha-Neto E: CD4+ T cell epitope discovery and rational vaccine design. Arch Immunol Ther Exp 58: 121-130, 2010.
34. Lo-Man R, Vichier-Guerre S, Bay S, Deriaud E, Cantacuzene D and Leclerc C: Antitumor immunity provided by a synthetic multiple antigenic glycopeptide displaying a tri-Tn glycotope. J Immunol 166: 2849-2854, 2001.
35. Singhal AK: Histo-blood group antigens in cancer. Semin Cancer Biol 2: 379-388, 1991.
36. Singh SK, Streng-Ouwehand I, Litjens M, et al: Characterization of murine MGL1 and MGL2 C-type lectins: distinct glycan specificities and tumor binding properties. Mol Immunol 46: 1240-1249, 2009.
37. Hubert P, Heitzmann A, Viel S, et al: Antibody-dependent cell cytotoxicity synapses form in mice during tumor-specific antibody immunotherapy. Cancer Res 71: 5134-5143, 2011.
38. Quezada SA, Simpson TR, Peggs KS, et al: Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J Exp Med 207: 637-650, 2010.
39. Baird JR, Byrne KT, Lizotte PH, et al: Immune-mediated regression of established B16F10 melanoma by intratumoral injection of attenuated Toxoplasma gondii protects against rechallenge. J Immunol 190: 469-478, 2013.
40. Villegas FR, Coca S, Villarrubia VG, et al: Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 35: 23-28, 2002.
41. Malhotra A and Shanker A: NK cells: immune cross-talk and therapeutic implications. Immunotherapy 3: 1143-1166, 2011.
42. Walzer T, Dalod M, Robbins SH, Zitvogel L and Vivier E: Natural-killer cells and dendritic cells: 'l'union fait la force'. Blood 106: 2252-2258, 2005.
43. Prestwich RJ, Errington F, Steele LP, et al: Reciprocal human dendritic cell-natural killer cell interactions induce antitumor activity following tumor cell infection by oncolytic reovirus. J Immunol 183: 4312-4321, 2009.
44. Gerosa F, Gobbi A, Zorzi P, et al: The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J Immunol 174: 727-734, 2005.
45. Blalock LT, Landsberg J, Messmer M, et al: Human dendritic cells adenovirally-engineered to express three defined tumor antigens promote broad adaptive and innate immunity. Oncoimmunology 1: 287-357, 2012.
46. van Die I, van Stijn CM, Geyer H and Geyer R: Structural and functional analysis of glycosphingolipids of Schistosoma mansoni. Methods Enzymol 480: 117-140, 2010.
47. Truchetet ME, Beven L, Renaudin H, et al: Potential role of Mycoplasma hominis in interleukin (IL)-17-producing CD4+ T-cell generation via induction of IL-23 secretion by human dendritic cells. J Infect Dis 204: 1796-1805, 2011.
48. Gowda DC: TLR-mediated cell signaling by malaria GPIs. Trends Parasitol 23: 596-604, 2007.
49. Campos MA, Almeida IC, Takeuchi O, et al: Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J Immunol 167: 416-423, 2001.
50. Junqueira C, Guerrero AT, Galvão-Filho B, et al: Trypanosoma cruzi adjuvants potentiate T cell-mediated immunity induced by a NY-ESO-1 based antitumor vaccine. PLoS One 7: e36245, 2012.
51. Tarang S, Kumar S and Batra SK: Mucins and toll-like receptors: kith and kin in infection and cancer. Cancer Lett 321: 110-119, 2012.
52. Freire T, Lo-Man R, Bay S and Leclerc C: Tn glycosylation of the MUC6 protein modulates its immunogenicity and promotes the induction of Th17-biased T cell responses. J Biol Chem 286: 7797-7811, 2011.