Enhanced therapeutic anti-tumor immunity induced by co-administration of 5-fluorouracil and adenovirus expressing CD40 ligand

Cancer Immunology, Immunotherapy

Volumn 63, Issue 3, 2014, Pages 273-282

  Liljenfeldt, Lina ^a   Gkirtzimanaki, Katerina ^b,c   Vyrla, Dimitra ^b,c   Svensson, Emma ^a   Loskog, Angelica Si ^a   Eliopoulos, Aristides G ^b,c  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF CRETE   (Greece)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

5 Fluorouracil; CD40L; Chemotherapy; Immunotherapy; Urinary bladder cancer

Indexed keywords

ADENOVIRIDAE; ANIMALS; ANTIBODY FORMATION; ANTIGENS, CD95; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CD40 LIGAND; CELL GROWTH PROCESSES; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; FAS LIGAND PROTEIN; FEMALE; FLUOROURACIL; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; RECOMBINANT PROTEINS; T-LYMPHOCYTES; URINARY BLADDER NEOPLASMS;

EID: 84894479967     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1507-6     Document Type: Article

References (46)

1. van Kooten C, Banchereau J (2000) CD40-CD40 ligand. J Leukoc Biol 67:2-17
2. Loskog AS, Eliopoulos AG (2009) The Janus faces of CD40 in cancer. Semin Immunol 21:301-307
3. Callard RE, Armitage RJ, Fanslow WC, Spriggs MK (1993) CD40 ligand and its role in X-linked hyper-IgM syndrome. Immunol Today 14:559-564
4. Hayward AR, Levy J, Facchetti F, Notarangelo L, Ochs HD, Etzioni A, Bonnefoy JY, Cosyns M, Weinberg A (1997) Cholangiopathy and tumors of the pancreas, liver, and biliary tree in boys with X-linked immunodeficiency with hyper-IgM. J Immunol 158:977-983
5. Mackey MF, Gunn JR, Maliszewsky C, Kikutani H, Noelle RJ, Barth RJ Jr (1998) Dendritic cells require maturation via CD40 to generate protective antitumor immunity. J Immunol 161:2094-2098
6. French RR, Chan HT, Tutt AL, Glennie MJ (1999) CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help. Nat Med 5:548-553
7. Kikuchi T, Crystal RG (1999) Anti-tumor immunity induced by in vivo adenovirus vector-mediated expression of CD40 ligand in tumor cells. Hum Gene Ther 10:1375-1387
8. Loskog A, Bjorkland A, Brown MP, Korsgren O, Malmstrom PU, Totterman TH (2001) Potent antitumor effects of CD154 transduced tumor cells in experimental bladder cancer. J Urol 166:1093-1097
9. Noguchi M, Imaizumi K, Kawabe T et al (2001) Induction of antitumor immunity by transduction of CD40 ligand gene and interferon-gamma gene into lung cancer. Cancer Gene Ther 8:421-429
10. Todryk SM, Tutt AL, Green MH, Smallwood JA, Halanek N, Dalgleish AG, Glennie MJ (2001) CD40 ligation for immunotherapy of solid tumours. J Immunol Methods 248:139-147
11. Dzojic H, Loskog A, Totterman TH, Essand M (2006) Adenovirus-mediated CD40 ligand therapy induces tumor cell apoptosis and systemic immunity in the TRAMP-C2 mouse prostate cancer model. Prostate 66:831-838
12. Sun Y, Peng D, Lecanda J, Schmitz V, Barajas M, Qian C, Prieto J (2000) In vivo gene transfer of CD40 ligand into colon cancer cells induces local production of cytokines and chemokines, tumor eradication and protective antitumor immunity. Gene Ther 7:1467-1476
13. Buhtoiarov IN, Lum H, Berke G, Paulnock DM, Sondel PM, Rakhmilevich AL (2005) CD40 ligation activates murine macrophages via an IFN-gamma-dependent mechanism resulting in tumor cell destruction in vitro. J Immunol 174:6013-6022
14. Sabel MS, Yamada M, Kawaguchi Y, Chen FA, Takita H, Bankert RB (2000) CD40 expression on human lung cancer correlates with metastatic spread. Cancer Immunol Immunother 49:101-108
15. Hirano A, Longo DL, Taub DD et al (1999) Inhibition of human breast carcinoma growth by a soluble recombinant human CD40 ligand. Blood 93:2999-3007
16. Tong AW, Papayoti MH, Netto G, Armstrong DT, Ordonez G, Lawson JM, Stone MJ (2001) Growth-inhibitory effects of CD40 ligand (CD154) and its endogenous expression in human breast cancer. Clin Cancer Res 7:691-703
17. Eliopoulos AG, Dawson CW, Mosialos G et al (1996) CD40-induced growth inhibition in epithelial cells is mimicked by Epstein-Barr Virus-encoded LMP1: involvement of TRAF3 as a common mediator. Oncogene 13:2243-2254
18. Knox PG, Davies CC, Ioannou M, Eliopoulos AG (2011) The death domain kinase RIP1 links the immunoregulatory CD40 receptor to apoptotic signaling in carcinomas. J Cell Biol 192:391-399
19. Afford SC, Randhawa S, Eliopoulos AG, Hubscher SG, Young LS, Adams DH (1999) CD40 activation induces apoptosis in cultured human hepatocytes via induction of cell surface fas ligand expression and amplifies fas-mediated hepatocyte death during allograft rejection. J Exp Med 189:441-446
20. Ghamande S, Hylander BL, Oflazoglu E, Lele S, Fanslow W, Repasky EA (2001) Recombinant CD40 ligand therapy has significant antitumor effects on CD40-positive ovarian tumor xenografts grown in SCID mice and demonstrates an augmented effect with cisplatin. Cancer Res 61:7556-7562
21. Moschonas A, Kouraki M, Knox PG, Thymiakou E, Kardassis D, Eliopoulos AG (2008) CD40 induces antigen transporter and immunoproteasome gene expression in carcinomas via the coordinated action of NF-kappaB and of NF-kappaB-mediated de novo synthesis of IRF-1. Mol Cell Biol 28:6208-6222
22. Gomes EM, Rodrigues MS, Phadke AP et al (2009) Antitumor activity of an oncolytic adenoviral-CD40 ligand (CD154) transgene construct in human breast cancer cells. Clin Cancer Res 15:1317-1325
23. Diaconu I, Cerullo V, Hirvinen ML et al (2012) Immune response is an important aspect of the antitumor effect produced by a CD40L-encoding oncolytic adenovirus. Cancer Res 72:2327-2338
24. Vonderheide RH, Butler MO, Liu JF, Battle TE, Hirano N, Gribben JG, Frank DA, Schultze JL, Nadler LM (2001) CD40 activation of carcinoma cells increases expression of adhesion and major histocompatibility molecules but fails to induce either CD80/CD86 expression or T cell alloreactivity. Int J Oncol 19:791-798
25. Malmstrom PU, Loskog AS, Lindqvist CA, Mangsbo SM, Fransson M, Wanders A, Gardmark T, Totterman TH (2010) AdCD40L immunogene therapy for bladder carcinoma: the first phase I/IIa trial. Clin Cancer Res 16:3279-3287
26. Beatty GL, Chiorean EG, Fishman MP et al (2011) CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331:1612-1616
27. Pesonen S, Diaconu I, Kangasniemi L et al (2012) Oncolytic immunotherapy of advanced solid tumors with a CD40L-expressing replicating adenovirus: assessment of safety and immunologic responses in patients. Cancer Res 72:1621-1631
28. Folkman J, Hahnfeldt P, Hlatky L (2000) Cancer: looking outside the genome. Nat Rev Mol Cell Biol 1:76-79
29. Loskog A, Dzojic H, Vikman S, Ninalga C, Essand M, Korsgren O, Totterman TH (2004) Adenovirus CD40 ligand gene therapy counteracts immune escape mechanisms in the tumor microenvironment. J Immunol 172:7200-7205
30. Jackaman C, Nelson DJ (2012) Intratumoral interleukin-2/agonist CD40 antibody drives CD4+ -independent resolution of treated-tumors and CD4+ -dependent systemic and memory responses. Cancer Immunol Immunother 61:549-560
31. Loskog AS, Fransson ME, Totterman TT (2005) AdCD40L gene therapy counteracts T regulatory cells and cures aggressive tumors in an orthotopic bladder cancer model. Clin Cancer Res 11:8816-8821
32. Eliopoulos AG, Wang CC, Dumitru CD, Tsichlis PN (2003) Tpl2 transduces CD40 and TNF signals that activate ERK and regulates IgE induction by CD40. EMBO J 22:3855-3864
33. Hannani D, Sistigu A, Kepp O, Galluzzi L, Kroemer G, Zitvogel L (2011) Prerequisites for the antitumor vaccine-like effect of chemotherapy and radiotherapy. Cancer J 17:351-358
34. Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9:162-174
35. Dolcetti L, Peranzoni E, Ugel S et al (2010) Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 40:22-35
36. Apetoh L, Ghiringhelli F, Tesniere A et al (2007) Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13:1050-1059
37. Tesniere A, Schlemmer F, Boige V et al (2010) Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 29:482-491
38. Ramakrishnan R, Gabrilovich DI (2013) Novel mechanism of synergistic effects of conventional chemotherapy and immune therapy of cancer. Cancer Immunol Immunother 62:405-410
39. Zitvogel L, Kepp O, Kroemer G (2011) Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 8:151-160
40. Nowak AK, Robinson BW, Lake RA (2003) Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res 63:4490-4496
41. Vardouli L, Lindqvist C, Vlahou K, Loskog AS, Eliopoulos AG (2009) Adenovirus delivery of human CD40 ligand gene confers direct therapeutic effects on carcinomas. Cancer Gene Ther 16:848-860
42. Vincent J, Mignot G, Chalmin F et al (2010) 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 70:3052-3061
43. Stewart TJ, Abrams SI (2008) How tumours escape mass destruction. Oncogene 27:5894-5903
44. Yeh KY, Pulaski BA, Woods ML, McAdam AJ, Gaspari AA, Frelinger JG, Lord EM (1995) B7-1 enhances natural killer cell-mediated cytotoxicity and inhibits tumor growth of a poorly immunogenic murine carcinoma. Cell Immunol 165:217-224
45. Cooke PW, James ND, Ganesan R, Wallace M, Burton A, Young LS (1999) CD40 expression in bladder cancer. J Pathol 188:38-43
46. Bugajska U, Georgopoulos NT, Southgate J, Johnson PW, Graber P, Gordon J, Selby PJ, Trejdosiewicz LK (2002) The effects of malignant transformation on susceptibility of human urothelial cells to CD40-mediated apoptosis. J Natl Cancer Inst 94:1381-1395