A pancreatic tumor-specific biomarker characterized in humans and mice as an immunogenic onco-glycoprotein is efficient in dendritic cell vaccination

Oncotarget

Volumn 6, Issue 27, 2015, Pages 23462-23479

  Collignon, Aurélie ^a   Perles Barbacaru, Adriana Teodora ^b   Robert, Stéphane ^c,d   Silvy, Françoise ^a   Martinez, Emmanuelle ^a   Crenon, Isabelle ^a   Germain, Sébastien ^a   Garcia, Stéphane ^c,e   Viola, Angèle ^b   Lombardo, Dominique ^a   Mas, Eric ^a   Béraud, Evelyne ^a  

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

^b University of Aix Marseille   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d INSERM   (France)

^e HÔPITAL NORD   (France)

Author keywords

Active immunotherapy; Biomarker; Cancer vaccines; Pancreatic cancer; Tumor associated antigen

Indexed keywords

DENDRITIC CELL VACCINE; GRANZYME B; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY J28; UNCLASSIFIED DRUG; CANCER VACCINE; CD3 ANTIGEN; EPITOPE; GLYCOPROTEIN; GRANZYME; TUMOR ANTIGEN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CANCER PREVENTION; CARBOXY TERMINAL SEQUENCE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG RESPONSE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREATIC CANCER CELL LINE; T LYMPHOCYTE ACTIVATION; TH1 CELL; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; CHEMISTRY; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EXPERIMENTAL MELANOMA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; METABOLISM; NUDE MOUSE; PANCREAS CARCINOMA; PANCREAS TUMOR; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CANCER VACCINES; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; DENDRITIC CELLS; EPITOPES; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; GLYCOSYLATION; GRANZYMES; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, NUDE; NEOPLASM TRANSPLANTATION; PANCREATIC NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84943377573     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4359     Document Type: Article

References (51)

1. Simard EP, Ward EM, Siegel R and Jemal A. Cancers with increasing incidence trends in the United States:1999 through 2008. CA:a Cancer Journal for Clinicians. 2012; 62:118-128.
2. Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM and Matrisian LM. Projecting cancer incidence and deaths to 2030:the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Research. 2011;74:2913-21.
3. Conroy T, Desseigne F, Ychou M, Bouché O, Guimbaud R, Bécouarn Y, Adenis A, Raoul JL, Gourgou-Bourgade S, de la Fouchardière C, Bennouna J, Bachet JB, KhemissaAkouz F, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. New England Journal of Medicine. 2011;364:1817-25.
4. Palucka K and Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity. 2013;39:38-48.
5. Vacchelli E, Vitale I, Eggermont A, Fridman WH, Fucíková J, Cremer I, Galon J, Tartour E, Zitvogel L, Kroemer G and Galluzzi L. Trial watch:Dendritic cell-based interventions for cancer therapy. Oncoimmunology. 2013;2:e25771.
6. Dodson LF, Hawkins WG and Goedegebuure P. Potential targets for pancreatic cancer immunotherapeutics. Immunotherapy. 2011;3:517-37.
7. 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. Journal of Biological Chemistry. 2011;286:7797-7811.
8. Ryan SO, Vlad AM, Islam K, Gariépy J and Finn OJ. Tumor-associated MUC1 glycopeptide epitopes are not subject to self-tolerance and improve responses to MUC1 peptide epitopes in MUC1 transgenic mice. Biological Chemistry. 2009;390:611-8.
9. Escribano MJ, Cordier J, Nap M, Ten Kate FJ and Burtin P. Differentiation antigens in fetal human pancreas. Reexpression in cancer. International Journal of Cancer. 1986;38:155-160.
10. Escribano MJ and Imperial S. Purification and molecular characterization of FAP, a feto-acinar protein associated with the differentiation of human pancreas. Journal of Biological Chemistry. 1989;264:21865-71.
11. Mas E, Abouakil N, Roudani S, Miralles F, Guy-Crotte O, Figarella C, Escribano MJ and Lombardo D. Human fetoacinar pancreatic protein:an oncofetal glycoform of the normally secreted pancreatic bile-salt-dependent lipase. Biochem Journal. 1993;289:609-615.
12. Franceschi C, Collignon A, Isnardon D, Benkoel L, Vérine A, Silvy F, Bernard JP, Lombardo D, Beraud E, Olive D and Mas E. A novel tumor-associated pancreatic glycoprotein is internalized by human dendritic cells and induces their maturation. Journal of Immunology. 2011;186:4067-77.
13. Panicot L, Mas E, Pasqualini E, Zerfaoui M, Lombardo D, Sadoulet MO and El Battari A. The formation of the oncofetal J28 glycotope involves core-2 beta6-N-acetylglucosaminyltransferase and alpha3/4-fucosyltransferase activities. Glycobiology. 1999;9(9):935-46.
14. Mas E, Crotte C, Lecestre D, Michalski JC, Escribano MJ, Lombardo D and Sadoulet MO. The oncofetal J28 epitope involves fucosylated O-linked oligosaccharide structures of the fetoacinar pancreatic protein. Glycobiology. 1997;7:745-52.
15. Panicot L, Mas E, Thivolet C and Lombardo D. Circulating antibodies against an exocrine pancreatic enzyme in type 1 diabetes. Diabetes. 1999;48:2316-23.
16. Aarnoudse CA, Garcia Vallejo JJ, Saeland E and van Kooyk Y. Recognition of tumor glycans by antigen-presenting cells. Current Opinion in Immunology. 2006;18:105-111.
17. Hiltbold EM, Vlad AM, Ciborowski P, Watkins SC and Finn OJ. The mechanism of unresponsiveness to circulating tumor antigen MUC1 is a block in intracellular sorting and processing by dendritic cells. Journal of Immunology. 2000;165:3730-41.
18. Beraud E, Collignon A, Franceschi C, Olive D, Lombardo D and Mas E. Investigation of a new tumor-associated glycosylated antigen as target for dendritic cell vaccination in pancreatic cancer. Oncoimmunology. 2012;1:56-61.
19. Panicot-Dubois L, Aubert M, Franceschi C, Mas E, Silvy F, Crotte C, Bernard J-P, Dominique Lombardo D and Sadoulet MO. 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. 2004;6:713-24.
20. Ryan SO, Vlad AM, Islam K, Gariépy J and Finn OJ. Tumor-associated MUC1 glycopeptide epitopes are not subject to self-tolerance and improve responses to MUC1 peptide epitopes in MUC1 transgenic mice. Biological Chemistry. 2009;390:611-8.
21. Mouchacca P, Schmitt-Verhulst AM and Boyer C. Visualization of cytolytic T cell differentiation and granule exocytosis with T cells from mice expressing active fluorescent granzyme B. PLoS One. 2013;8:e67239.
22. Hernell O and Bläckberg L. Human milk bile saltstimulated lipase:functional and molecular aspects. Journal of Pediatrics. 1994;125:56-61.
23. Steinman RM and Banchereau J. Taking dendritic cells into medicine. Nature. 2007;449:419-26.
24. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nature Reviews Immunology. 2003;3:133-46.
25. Ma A, Koka R and Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annual Review of Immunology. 2006;24:657-79.
26. Bonmort M, Dalod M, Mignot G, Ullrich E, Chaput N and Zitvogel L. Killer dendritic cells:IKDC and the others. Current Opinion in Immunology. 2008;20:558-65.
27. Tel J, Anguille S, Waterborg CE, Smits EL, Figdor CG and de Vries IJ. Tumoricidal activity of human dendritic cells. Trends in Immunology. 2014;35:38-46.
28. Prins RM, Odesa SK and Liau LM. Immunotherapeutic targeting of shared melanoma-associated antigens in a murine glioma model. Cancer Research. 2003;63:8487-91.
29. Kim HS, Choo YS, Koo T, Bang S, Oh TY, Wen J and Song SY. Enhancement of antitumor immunity of dendritic cells pulsed with heat-treated tumor lysate in murine pancreatic cancer. Immunology Letters. 2006;103:142-48.
30. Bauer C, Bauernfeind F, Sterzik A, Orban M, Schnurr M, Lehr HA, Endres S, Eigler A and Dauer M. Dendritic cellbased vaccination combined with gemcitabine increases survival in a murine pancreatic carcinoma model. Gut. 2007;56:1275-82.
31. Schmidt T, Marten A, Endres S, Tiemann K, Schmitz V, Gorschlüter M, Schneider C, Sauerbruch T and SchmidtWolf IG. Intratumoral immunization with tumor RNApulsed dendritic cells confers antitumor immunity in a C57BL/6 pancreatic murine tumor model. Cancer Research. 2003;63:8962-67.
32. Eberl G, Brawand P and MacDonald HR. Selective bystander proliferation of memory CD4+ and CD8+ T cells upon NK T or T cell activation. Journal of Immunology. 2000;165:4305-11.
33. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM and Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331:44-9.
34. Carreno BM, Becker-Hapak M, Huang A, Chan M, Alyasiry A, Lie WR, Aft RL, Cornelius LA, Trinkaus KM and Linette GP. IL-12p70-producing patient DC vaccine elicits Tc1-polarized immunity. Journal of Clinical Investigation. 2013;123:3383-94.
35. Lion E, Smits EL, Berneman ZN and Van Tendeloo VF. NK cells:key to success of DC-based cancer vaccines? The Oncologist. 2012;17:1256-70.
36. Leung W. Infusions of Allogeneic Natural Killer Cells as Cancer Therapy. Clinical Cancer Research. 2014;20:3390-400.
37. Wargo JA, Schumacher LY, Comin-Anduix B, Dissette VB, Glaspy JA, McBride WH, Butterfield LH, Economou JS and Ribas A. Natural killer cells play a critical role in the immune response following immunization with melanomaantigen-engineered dendritic cells. Cancer Gene Therapy. 2005;12:516-27.
38. Boudreau JE, Bridle BW, Stephenson KB, Jenkins KM, Brunellière J, Bramson JL, Lichty BD and Wan Y. Recombinant vesicular stomatitis virus transduction of dendritic cells enhances their ability to prime innate and adaptive antitumor immunity. Molecular Therapy. 2009;17:1465-72.
39. Ribas A, Wargo JA, Comin-Anduix B, Sanetti S, Schumacher LY, McLean C, Dissette VB, Glaspy JA, McBride WH, Butterfield LH and Economou JS. Enhanced tumor responses to dendritic cells in the absence of CD8-positive cells. Journal of Immunology. 2004;172:4762-69.
40. Shimizu K and Fujii S. DC therapy induces long-term NK reactivity to tumors via host DC. European Journal of Immunology. 2009;39:457-68.
41. Boudreau JE, Stephenson KB, Wang F, Jenkins KM, Brunellière J, Bramson JL, Lichty BD and Wan Y. IL-15 and type I interferon are required for activation of tumoricidal NK cells by virus-infected dendritic cells. Cancer Research. 2011;71:2497-506.
42. Candido KA, Shimizu K, McLaughlin JC, Kunkel R, Fuller JA, Redman BG, Thomas EK, Nickoloff BJ and Mulé JJ. Local administration of dendritic cells inhibits established breast tumor growth:implications for apoptosis-inducing agents. Cancer Research. 2001;61:228-36.
43. Vincent A, Herman J, Schulick R, Hruban RH and Goggins M. Pancreatic cancer. Lancet. 2011;378:607-20.
44. Aguirre AJ, Bardeesy N, Sinha M, Tuveson DA, Horner J, Redston MS and DePinho RA. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes and Development. 2003;17:3112-26.
45. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, Rustgi AK, Chang S and Tuveson DA. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell. 2005;7:469-83.
46. Blackford A, Parmigiani G, Kensler TW, Wolfgang C, Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Eshleman JR, Goggins M, Jaffee EM, Iacobuzio-Donahue CA, et al. Genetic mutations associated with cigarette smoking in pancreatic cancer. Cancer Research. 2009;69:3681-3688.
47. Seelig SK, Burkert B, Chromik AM, Tannapfel A, Uhl Wand Seelig MH. Pancreatic resections for advanced M1-pancreatic carcinoma:the value of synchronous metastasectomy. HPB Surgery. 2010;2010:579-672.
48. van den Broeck A, Sergeant G, Ectors N, Van Steenbergen W, Aerts R and Topal B. Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma. European Journal of Surgical Oncology. 2009;35:600-4.
49. Melero I, Gaudernack G, Gerritsen W, Huber C, Parmiani G, Scholl S, Thatcher N, Wagstaff J, Zielinski C, Faulkner I and Mellstedt H. Therapeutic vaccines for cancer:an overview of clinical trials. Nature Reviews Clinical Oncology. 2014;11:509-24.
50. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S and Steinman R M. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. Journal of Experimental Medicine. 1992;176:1693-1702.
51. Conductier G*, Brau F*, Viola A*, Langlet F, Ramkumar N, Dehouck B, Lemaire T, Chapot R, Lucas L, Rovère C, Maitre P, Hosseiny S, Petit-Paitel A, et al. Melaninconcentrating hormone regulates beat frequency of ependymal cilia and ventricular volume. Nature Neuroscience. 2013;16:845-7 (* first co-authors).