Combination of an agonistic anti-CD40 monoclonal antibody and the COX-2 inhibitor celecoxib induces anti-glioma effects by promotion of type-1 immunity in myeloid cells and T-cells

Cancer Immunology, Immunotherapy

Volumn 63, Issue 8, 2014, Pages 847-857

  Kosaka, Akemi ^a,b   Ohkuri, Takayuki ^a,b   Okada, Hideho ^a,b  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Agonistic anti CD40 mAb; Celecoxib; COX 2; Glioma; Myeloid cells; Type 1 immunity

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD40 MONOCLONAL ANTIBODY; CD8 ANTIGEN; CELECOXIB; CYCLOOXYGENASE 2; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MONOCLONAL ANTIBODY; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; BRAIN; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MATURATION; CELL SELECTION; CONTROLLED STUDY; FEMALE; GLIOMA; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN; SURVIVAL; THERAPY EFFECT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD40; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CYCLOOXYGENASE 2 INHIBITORS; FEMALE; GLIOMA; MICE; MICE, INBRED C57BL; MYELOID CELLS; PYRAZOLES; RATS; SULFONAMIDES; T-LYMPHOCYTES, CYTOTOXIC; TRANSFECTION;

EID: 84906791903     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1561-8     Document Type: Article

References (50)

1. Ostrom QT, Gittleman H, Farah P, Ondracek A, Chen Y, Wolinsky Y, Stroup NE, Kruchko C, Barnholtz-Sloan JS (2013) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2006-2010. Neuro Oncol 15:ii1-ii56
2. Jovčevska I, Kočevar N, Komel R (2013) Glioma and glioblastoma - how much do we (not) know? Mol Clin Oncol 1:935-941
3. Allavena P, Mantovani A (2012) Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 167:195-205
4. Schmieder A, Michel J, Schonhaar K, Goerdt S, Schledzewski K (2012) Differentiation and gene expression profile of tumor-associated macrophages. Semin Cancer Biol 22:289-297
5. Khaled YS, Ammori BJ, Elkord E (2013) Myeloid-derived suppressor cells in cancer: recent progress and prospects. Immunol Cell Biol 91:493-502
6. Grewal IS, Flavell RA (1998) CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol 16:111-135 (Pubitemid 28183361)
7. Kato T, Hakamada R, Yamane H, Nariuchi H (1996) Induction of IL-12 p40 messenger RNA expression and IL-12 production of macrophages via CD40-CD40 ligand interaction. J Immunol 156:3932-3938 (Pubitemid 26139944)
8. Koch F, Stanzl U, Jennewein P, Janke K, Heufler C, Kämpgen E, Romani N, Schuler G (1996) High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med 184:741-746 (Pubitemid 26324128)
9. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 184:747-752 (Pubitemid 26324129)
10. Lum HD, Buhtoiarov IN, Schmidt BE, Berke G, Paulnock DM, Sondel PM, Rakhmilevich AL (2006) Tumoristatic effects of anti-CD40 mAb-activated macrophages involve nitric oxide and tumour necrosis factor-alpha. Immunology 118:261-270 (Pubitemid 43727432)
11. 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 (Pubitemid 40663788)
12. Lum HD, Buhtoiarov IN, Schmidt BE, Berke G, Paulnock DM, Sondel PM, Rakhmilevich AL (2006) In vivo CD40 ligation can induce T cell-independent antitumor effects that involve macrophages. J Leukoc Biol 79:1181-1192 (Pubitemid 44835552)
13. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, Huhn RD, Song W, Li D, Sharp L, Torigian DA, O'Dwyer PJ, Vonderheide RH (2011) CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331:1612-1616
14. Eruslanov E, Kaliberov S, Daurkin I, Kaliberova L, Buchsbaum D, Vieweg J, Kusmartsev S (2009) Altered expression of 15-hydroxyprostaglandin dehydrogenase in tumor-infiltrated CD11b myeloid cells: a mechanism for immune evasion in cancer. J Immunol 182:7548-7557
15. Eruslanov E, Daurkin I, Vieweg J, Daaka Y, Kusmartsev S (2011) Aberrant PGE2 metabolism in bladder tumor microenvironment promotes immunosuppressive phenotype of tumor-infiltrating myeloid cells. Int Immunopharmacol 11:848-855
16. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S (2007) Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 67:4507-4513 (Pubitemid 46815102)
17. Veltman JD, Lambers ME, van Nimwegen M, Hendriks RW, Hoogsteden HC, Aerts JG, Hegmans JP (2010) COX-2 inhibition improves immunotherapy and is associated with decreased numbers of myeloid-derived suppressor cells in mesothelioma. Celecoxib influences MDSC function. BMC Cancer 10:464
18. Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, Ohlfest JR, Okada H (2011) COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res 71:2664-2674
19. Wiesner SM, Decker SA, Larson JD, Ericson K, Forster C, Gallardo JL, Long C, Demorest ZL, Zamora EA, Low WC, SantaCruz K, Largaespada DA, Ohlfest JR (2009) De novo induction of genetically engineered brain tumors in mice using plasmid DNA. Cancer Res 69:431-439
20. Litterman AJ, Zellmer DM, Grinnen KL, Hunt MA, Dudek AZ, Salazar AM, Ohlfest JR (2013) Profound impairment of adaptive immune responses by alkylating chemotherapy. J Immunol 190:6259-6268
21. Nishimura F, Dusak JE, Eguchi J, Zhu X, Gambotto A, Storkus WJ, Okada H (2006) Adoptive transfer of type 1 CTL mediates effective anti-central nervous system tumor response: critical roles of IFN-inducible protein-10. Cancer Res 66:4478-4487
22. Sedgwick JD, Schwender S, Imrich H, Dörries R, Butcher GW, ter Meulen V (1991) Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci USA 88:7438-7442 (Pubitemid 21915167)
23. Umemura N, Saio M, Suwa T, Kitoh Y, Bai J, Nonaka K, Ouyang GF, Okada M, Balazs M, Adany R, Shibata T, Takami T (2008) Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J Leukoc Biol 83:1136-1144 (Pubitemid 351960345)
24. Luster AD, Unkeless JC, Ravetch JV (1985) Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature 315:672-676 (Pubitemid 15232881)
25. Narumi S, Hamilton TA (1991) Inducible expression of murine IP-10 mRNA varies with the state of macrophage inflammatory activity. J Immunol 146:3038-3044
26. Munder M (2009) Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158:638-651
27. von Leoprechting A, van der Bruggen P, Pahl HL, Aruffo A, Simon JC (1999) Stimulation of CD40 on immunogenic human malignant melanomas augments their cytotoxic T lymphocyte-mediated lysis and induces apoptosis. Cancer Res 59:1287-1294 (Pubitemid 29136260)
28. French R, Chan HT, Turr 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 (Pubitemid 29220214)
29. Alexandroff AB, Jackson AM, Paterson T, Haley JL, Ross JA, Longo DL, Murphy WJ, James K, Taub DD (2000) Role for CD40-CD40 ligand interactions in the immune response to solid tumours. Mol Immunol 37:515-526 (Pubitemid 32001693)
30. 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 (Pubitemid 32167031)
31. van Mierlo GJ, den Boer AT, Medema JP, van der Voort EI, Fransen MF, Offringa R, Melief CJ, Toes RE (2002) CD40 stimulation leads to effective therapy of CD40(-) tumors through induction of strong systemic cytotoxic T lymphocyte immunity. Proc Natl Acad Sci USA 99:5561-5566 (Pubitemid 34411588)
32. Wischhusen J, Schnider D, Mittelbronn M, Meyermann R, Engelmann H, Jung G, Wiendl H, Weller M (2005) Death receptormediated apoptosis in human malignant glioma cells: modulation by the CD40/CD40L system. J Neuroimmunol 162:28-42
33. Xie F, Shi Q, Wang Q, Ge Y, Chen Y, Zuo J, Gu Y, Deng H, Mao H, Hu Z, Zhou Y, Zhang X (2010) CD40 is a regulator for vascular endothelial growth factor in the tumor microenvironment of glioma. J Neuroimmunol 222:62-69
34. Vonderheide RH, Bajor DL, Winograd R, Evans RA, Bayne LJ, Beatty GL (2013) CD40 immunotherapy for pancreatic cancer. Cancer Immunol Immunother 62:949-954
35. Turner JG, Rakhmilevich AL, Burdelya L, Neal Z, Imboden M, Sondel PM, Yu H (2001) Anti-CD40 antibody induces antitumor and antimetastatic effects: the role of NK cells. J Immunol 166:89-94 (Pubitemid 32038420)
36. Masferrer JL, Zweifel BS, Manning PT, Hauser SD, Leahy KM, Smith WG, Isakson PC, Seibert K (1994) Selective inhibition of inducible cyclooxygenase 2 in vivo is antiinflammatory and non-ulcerogenic. Proc Natl Acad Sci USA 91:3228-3232 (Pubitemid 24130209)
37. Ohmori Y, Hamilton TA (1994) Cell type and stimulus specific regulation of chemokine gene expression. Biochem Biophys Res Commun 198:590-596 (Pubitemid 24178409)
38. Neville LF, Mathiak G, Bagasra O (1997) The immunobiology of interferon-gamma inducible protein 10 kD (IP-10): a novel, pleiotropic member of the C-X-C chemokine superfamily. Cytokine Growth Factor Rev 8:207-219 (Pubitemid 28077928)
39. Liu M, Guo S, Hibbert JM, Jain V, Singh N, Wilson NO, Stiles JK (2011) CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine Growth Factor Rev 22:121-130
40. Antonelli A, Ferrari SM, Giuggioli D, Ferrannini E, Ferri C, Fallahi P (2014) Chemokine (C-X-C motif) ligand (CXCL)10 in autoimmune diseases. Autoimmun Rev 13:272-280
41. Enderlin M, Kleinmann EV, Struyf S, Buracchi C, Vecchi A, Kinscherf R, Kiessling F, Paschek S, Sozzani S, Rommelaere J, Cornelis JJ, Van Damme J, Dinsart C (2009) TNF-alpha and the IFN-gamma-inducible protein 10 (IP-10/CXCL-10) delivered by parvoviral vectors act in synergy to induce antitumor effects in mouse glioblastoma. Cancer Gene Ther 16:149-160
42. Jiang XB, Lu XL, Hu P, Liu RE (2009) Improved therapeutic efficacy using vaccination with glioma lysate-pulsed dendritic cells combined with IP-10 in murine glioma. Vaccine 27:6210-6216
43. Fujita M, Zhu X, Ueda R, Sasaki K, Kohanbash G, Kastenhuber ER, McDonald HA, Gibson GA, Watkins SC, Muthuswamy R, Kalinski P, Okada H (2009) Effective immunotherapy against murine gliomas using type 1 polarizing dendritic cells - significant roles of CXCL10. Cancer Res 69:1587-1595
44. Fujita M, Zhu X, Sasaki K, Ueda R, Low KL, Pollack IF, Okada H (2008) Inhibition of STAT3 promotes the efficacy of adoptive transfer therapy using type-1 CTLs by modulation of the immunological microenvironment in a murine intracranial glioma. J Immunol 180:2089-2098
45. Rodriguez PC, Hernandez CP, Quiceno D, Dubinett SM, Zabaleta J, Ochoa JB, Gilbert J, Ochoa AC (2005) Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med 202:931-939 (Pubitemid 41396893)
46. Prins RM, Odesa SK, Liau LM (2003) Immunotherapeutic targeting of shared melanoma-associated antigens in a murine glioma model. Cancer Res 63:8487-8491 (Pubitemid 37549505)
47. Hatano M, Kuwashima N, Tatsumi T, Dusak JE, Nishimura F, Reilly KM, Storkus WJ, Okada H (2004) Vaccination with EphA2-derived T cell-epitopes promotes immunity against both EphA2-expressing and EphA2-negative tumors. J Transl Med 2:40
48. Iizuka Y, Kojima H, Kobata T, Kawase T, Kawakami Y, Toda M (2006) Identification of a glioma antigen, GARC-1, using cytotoxic T lymphocytes induced by HSV cancer vaccine. Int J Cancer 118:942-949 (Pubitemid 43157669)
49. Ohlfest JR, Andersen BM, Litterman AJ, Xia J, Pennell CA, Swier LE, Salazar AM, Olin MR (2013) Vaccine injection site matters: qualitative and quantitative defects in CD8 T cells primed as a function of proximity to the tumor in a murine glioma model. J Immunol 190:613-620
50. Calzascia T, Masson F, Di Berardino-Besson W, Contassot E, Wilmotte R, Aurrand-Lions M, Rüegg C, Dietrich PY, Walker PR (2005) Homing phenotypes of tumor-specific CD8 T cells are predetermined at the tumor site by crosspresenting APCs. Immunity 22:175-184 (Pubitemid 40255709)