Chemo-immunotherapy mediates durable cure of orthotopic KrasG12D/p53−/− pancreatic ductal adenocarcinoma

OncoImmunology

Volumn 5, Issue 9, 2016, Pages

  Konduri, Vanaja ^a   Li, Dali ^a   Halpert, Matthew M ^a   Liang, Dan ^a   Liang, Zhengdong ^a   Chen, Yunyu ^a   Fisher, William E ^a   Paust, Silke ^a   Levitt, Jonathan M ^a   Yao, Qizhi Cathy ^a,b   Decker, William K ^a,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

Adjuvant therapy; PDAC; tumor immunology; vaccination

Indexed keywords

GEMCITABINE; K RAS PROTEIN; PROTEIN P53;

ARTICLE; CANCER CHEMOTHERAPY; CD8+ T LYMPHOCYTE; CELL MANIPULATION; CELLULAR IMMUNITY; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL; T LYMPHOCYTE; TUMOR GROWTH; VACCINATION; WESTERN BLOTTING;

EID: 84986274982     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1213933     Document Type: Article

References (54)

1. D.Ansari, A.Gustafsson, R.Anderson. Update on the management of pancreatic cancer:surgery is not enough. World J Gastroenterol 2015; 21:3157-65; PMID:25805920; http://dx.doi.org/10.3748/wjg.v21.i11.3157
2. M.D.Fesinmeyer, M.A.Austin, C.I.Li, A.J.De Roos, D.J.Bowen. Differences in survival by histologic type of pancreatic cancer. Cancer Epidemiol Biomarkers Prev 2005; 14:1766-73; PMID:16030115; http://dx.doi.org/10.1158/1055-9965.EPI-05-0120
3. American Cancer Society. Cancer Facts & Figures 2016. Atlanta:American Cancer Society; 2016
4. E.Niccolai, D.Prisco, M.M.D'Elios, A.Amedei. What is recent in pancreatic cancer immunotherapy? Biomed Res Int 2013; 2013:492372; PMID:23509731; http://dx.doi.org/10.1155/2013/492372
5. A.J.Lepisto, A.J.Moser, H.Zeh, K.Lee, D.Bartlett, J.R.McKolanis, B.A.Geller, A.Schmotzer, D.P.Potter, T.Whiteside. A phase I/II study of a MUC1 peptide pulsed autologous dendritic cell vaccine as adjuvant therapy in patients with resected pancreatic and biliary tumors. Cancer Ther 2008; 6:955-64; PMID:19129927
6. M.A.Morse, S.K.Nair, D.Boczkowski, D.Tyler, H.I.Hurwitz, A.Proia, T.M.Clay, J.Schlom, E.Gilboa, H.K.Lyerly. The feasibility and safety of immunotherapy with dendritic cells loaded with CEA mRNA following neoadjuvant chemoradiotherapy and resection of pancreatic cancer. Int J Gastrointest Cancer 2002; 32:1-6; PMID:12630764; http://dx.doi.org/10.1385/IJGC:32:1:1
7. M.F.Kalady, M.W.Onaitis, S.Emani, Z.Abdul-Wahab, S.K.Pruitt, D.S.Tyler. Dendritic cells pulsed with pancreatic cancer total tumor RNA generate specific antipancreatic cancer T cells. J Gastrointest Surg 2004; 8:175-81; PMID:15036193; http://dx.doi.org/10.1016/j.gassur.2003.11.003
8. Y.Akiyama, K.Maruyama, N.Nara, T.Hojo, J.Y.Cheng, T.Mori, R.H.Wiltrout, K.Yamaguchi. Antitumor effects induced by dendritic cell-based immunotherapy against established pancreatic cancer in hamsters. Cancer Lett 2002; 84:37-47; PMID:12104046; http://dx.doi.org/10.1016/S0304-3835(02)00189-1
9. D.T.Le, E.Lutz, J.N.Uram, E.A.Sugar, B.Onners, S.Solt, L.Zheng, L.A.DiazJr, R.C.Donehower, E.M.Jaffee et al. Evaluation of ipilimumab in combination with allogeneic pancreatic tumor cells transfected with a GM-CSF gene in previously treated pancreatic cancer. J Immunother 2013; 36:382-9; PMID:23924790; http://dx.doi.org/10.1097/CJI.0b013e31829fb7a2
10. T.Kammertoens, T.Schuler, T.Blankenstein. Immunotherapy:target the stroma to hit the tumor. Trends Mol Med 2005; 11:225-31; PMID:15882610; http://dx.doi.org/10.1016/j.molmed.2005.03.002
11. M.M.Halpert, V.Konduri, D.Liang, Y.Chen, J.B.Wing, S.Paust, J.M.Levitt, W.K.Decker. Dendritic cell secreted CTLA-4 regulates the T-cell response by downmodulating bystander surface B7. Stem Cells Dev 2016; 15:774-87; PMID:26979751; http://dx.doi.org/10.1089/scd.2016.0009
12. W.Cheng, X.Ren, C.Zhang, J.Cai, Y.Liu, S.Han, A.Wu. Bioinformatic profiling identifies an immune-related risk signature for glioblastoma. Neurology 2016; 86:2226-34; PMID:27225222; http://dx.doi.org/10.1212/WNL.0000000000002770
13. D.Liang, M.M.Halpert, V.Konduri, W.K.Decker. Stepping out of the cytosol:AIMp1/p43 potentiates the link between innate and adaptive immunity. Int Rev Immunol 2015; 34:367-81; PMID:26325028; http://dx.doi.org/10.3109/08830185.2015.1077829
14. H2 immune responses. Clin Immunol 2012; 143:256-65; PMID:22472603; http://dx.doi.org/10.1016/j.clim.2012.02.004
15. E.Kim, S.H.Kim, S.Kim, D.Cho, T.S.Kim. AIMP1/p43 protein induces the maturation of bone marrow-derived dendritic cells with T helper type 1-polarizing ability. J Immunol 2008; 180:2894-902; PMID:18292511; http://dx.doi.org/10.4049/jimmunol.180.5.2894
16. W.K.Decker, D.Xing, S.Li, S.N.Robinson, H.Yang, D.Steiner, K.V.Komanduri, E.J.Shpall. Th-1 polarization is regulated by dendritic cell comparison of MHC class I and class II antigens. Blood 2009; 113:4213-23; PMID:19171878; http://dx.doi.org/10.1182/blood-2008-10-185470
17. W.K.Decker, D.Xing, S.Li, S.N.Robinson, H.Yang, X.Yao, H.Segall, J.D.McMannis, K.V.Komanduri, R.E.Champlin et al. Double loading of dendritic cell MHC class I and class II with an AML antigen repertoire enhances correlates of T-cell immunity in vitro via amplification of T-cell help. Vaccine 2006; 24:3203-16; PMID:16480795; http://dx.doi.org/10.1016/j.vaccine.2006.01.029
18. H1 immunity. Submitted.
19. R.Jalah, M.Rosati, B.Ganneru, G.R.Pilkington, A.Valentin, V.Kulkarni, C.Bergamaschi, B.Chowdhury, G.M.Zhang, R.K.Beach et al. The p40 subunit of interleukin (IL)-12 promotes stabilization and export of the p35 subunit. J Biol Chem 2013; 288:6763-76; PMID:23297419; http://dx.doi.org/10.1074/jbc.M112.436675
20. + T cells escape TGF-β control and contribute to early microbial pathogen response. Nat Commun 2014; 5:5150; PMID:25284210; http://dx.doi.org/10.1038/ncomms6150
21. + T lymphocytes mediate lung allograft acceptance. J Clin Invest 2014; 124:1130-43; PMID:24569377; http://dx.doi.org/10.1172/JCI71359
22. + T cell-responses by IL-10 dependent mechanism during H5N1 influenza virus infection. Eur J Immunol 2014; 44:103-14; PMID:24114149; http://dx.doi.org/10.1002/eji.201343583
23. M.Dauer, J.Herten, C.Bauer, F.Renner, K.Schad, M.Schnurr, S.Endres, A.Eigler. Chemosensitization of pancreatic carcinoma cells to enhance T cell-mediated cytotoxicity induced by tumor lysate-pulsed dendritic cells. J Immunother 2005; 28:332-42; PMID:16000951; http://dx.doi.org/10.1097/01.cji.0000164038.41104.f5
24. H.S.Kim, Y.S.Choo, T.Koo, S.Bang, T.Y.Oh, J.Wen, S.Y.Song. Enhancement of antitumor immunity of dendritic cells pulsed with heat-treated tumor lysate in murine pancreatic cancer. Immunol Lett 2006; 103:142-8; PMID:16313973; http://dx.doi.org/10.1016/j.imlet.2005.10.021
25. T.Schmidt, C.Ziske, A.Marten, S.Endres, K.Tiemann, V.Schmitz, M.Gorschlüter, C.Schneider, T.Sauerbruch, I.G.Schmidt-Wolf. Intratumoral immunization with tumor RNA-pulsed dendritic cells confers antitumor immunity in a C57BL/6 pancreatic murine tumor model. Cancer Res 2003; 63:8962-8967; PMID:14695214
26. S.K.Nair, S.Hull, D.Coleman, E.Gilboa, H.K.Lyerly, M.A.Morse. Induction of carcinoembryonic antigen (CEA)-specific cytotoxic T-lymphocyte responses in vitro using autologous dendritic cells loaded with CEA peptide or CEA RNA in patients with metastatic malignancies expressing CEA. Int J Cancer 1999; 82:121-124; PMID:10360830; http://dx.doi.org/10.1002/(SICI)1097-0215(19990702)82:1%3c121::AID-IJC20%3e3.0.CO;2-X
27. J.J.Mule. Dendritic cell-based vaccines for pancreatic cancer and melanoma. Ann NY Acad Sci 2009; 1174:33-40; PMID:19769734; http://dx.doi.org/10.1111/j.1749-6632.2009.04936.x
28. S.Mosolits, G.Ullenhag, H.Mellstedt. Therapeutic vaccination in patients with gastrointestinal malignancies. A review of immunological and clinical results. Ann Oncol 2005; 16:847-62; PMID:15829493; http://dx.doi.org/10.1093/annonc/mdi192
29. S.Broomfield, A.Currie, R.G.van der Most, M.Brown, I.van Bruggen, B.W.Robinson, R.A.Lake. Partial, but not complete, tumor-debulking surgery promotes protective antitumor memory when combined with chemotherapy and adjuvant immunotherapy. Cancer Res 2005; 65:7580-4; PMID:16140921
30. P.Correale, M.G.Cusi, K.Y.Tsang, M.T.Del Vecchio, S.Marsili, M.L.Placa, C.Intrivici, A.Aquino, L.Micheli, C.Nencini et al. Chemo-immunotherapy of metastatic colorectal carcinoma with gemcitabine plus FOLFOX 4 followed by subcutaneous granulocyte macrophage colony-stimulating factor and interleukin-2 induces strong immunologic and antitumor activity in metastatic colon cancer patients. J Clin Oncol 2005; 23:8950-8; PMID:16061910; http://dx.doi.org/10.1200/JCO.2005.12.147
31. + myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res 2005; 11:6713-21; PMID:16166452; http://dx.doi.org/10.1158/1078-0432.CCR-05-0883
32. P.Sinha, V.K.Clements, S.K.Bunt, S.M.Albelda, S.Ostrand-Rosenberg. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 2007; 179:977-83; PMID:17617589; http://dx.doi.org/10.4049/jimmunol.179.2.977
33. H.K.Le, L.Graham, E.Cha, J.K.Morales, M.H.Manjili, H.D.Bear. Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunopharmacol 2009; 9:900-9; PMID:19336265; http://dx.doi.org/10.1016/j.intimp.2009.03.015
34. + dendritic cells in patients with advanced pancreatic cancer. Jpn J Clin Oncol 2009; 39:797-806; PMID:19797418; http://dx.doi.org/10.1093/jjco/hyp112
35. C.Bauer, F.Bauernfeind, A.Sterzik, M.Orban, M.Schnurr, H.A.Lehr, S.Endres, A.Eigler, M.Dauer. Dendritic cell-based vaccination combined with gemcitabine increases survival in a murine pancreatic carcinoma model. Gut 2007; 56:1275-82; PMID:17395611; http://dx.doi.org/10.1136/gut.2006.108621
36. G.L.Beatty, E.G.Chiorean, M.P.Fishman, B.Saboury, U.R.Teitelbaum, W.Sun, R.D.Huhn, W.Song, D.Li, L.L.Sharp et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011; 331:1612-6; PMID:21436454; http://dx.doi.org/10.1126/science.1198443
37. A.K.Nowak, B.W.Robinson, R.A.Lake. Gemcitabine exerts a selective effect on the humoral immune response:implications for combination chemo-immunotherapy. Cancer Res 2002; 62:2353-8; PMID:11956096
38. A.K.Nowak, R.A.Lake, A.L.Marzo, B.Scott, W.R.Heath, E.J.Collins, J.A.Frelinger, B.W.Robinson. Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross tolerizing host tumor-specific CD8 T cells. J Immunol 2003; 170:4905-13; PMID:12734333; http://dx.doi.org/10.4049/jimmunol.170.10.4905
39. J.M.Plate, A.E.Plate, S.Shott, S.Bograd, J.E.Harris. Effect of gemcitabine on immune cells in subjects with adenocarcinoma of the pancreas. Cancer Immunol Immunother 2005; 54:915-25; PMID:15782312; http://dx.doi.org/10.1007/s00262-004-0638-1
40. W.M.Yokoyama, W.Seaman. The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells:the NK gene complex. Annu Rev Immunol 1993; 11:613; PMID:8476574; http://dx.doi.org/10.1146/annurev.iy.11.040193.003145
41. J.C.Ryan, J.Turck, E.C.Niemi, W.M.Yokoyama, W.E.Seaman. Molecular cloning of the NK1.1 antigen, a member of the NKR-P1 family of natural killer cell activation molecules. J Immunol 1992; 149:1631; PMID:1506685
42. J.C.Ryan, W.E.Seaman. Divergent functions of lectin-like receptors on NK cells. Immunol Rev 1997; 155:79; PMID:9059884; http://dx.doi.org/10.1111/j.1600-065X.1997.tb00941.x
43. J.R.Carlyle, A.Martin, A.Mehra, L.Attisano, F.W.Tsui, J.C.Zúñiga-Pflücker. Mouse NKR-P1B, a novel NK1.1 antigen with inhibitory function. J Immunol 1999; 162:5917; PMID:10229828
44. S.K.Kung, R.C.Su, J.Shannon, R.G.Miller. The NKR-P1B gene product is an inhibitory receptor on SJL/J NK cells. J Immunol 1999; 162:5876; PMID:10229823
45. G.C.Koo, F.J.Dumont, M.Tutt, J.HackettJr, V.Kumar. The NK-1.12 mouse:a model to study differentiation of murine NK cells. J Immunol 1986; 137:3742; PMID:3782794
46. H.Arase, N.Arase, T.Saito. Interferon-g production by natural killer (NK) cells and NK1.11 T cells upon NKR-P1 cross-linking. J Exp Med 1996; 183:2391; PMID:8642351; http://dx.doi.org/10.1084/jem.183.5.2391
47. A.Reichlin, W.M.Yokoyama. Natural killer cell proliferation induced by anti-NK1.1 and IL-2. Immunol Cell Biol 1998; 76:143; PMID:9619484; http://dx.doi.org/10.1046/j.1440-1711.1998.00726.x
48. + T cells rapidly acquire NK1.1 and NK cell-associated molecules upon stimulation in vitro and in vivo. J Immunol 2000; 165:3673-9; PMID:11034371; http://dx.doi.org/10.4049/jimmunol.165.7.3673
49. F.J.Kos, E.G.Engleman. Role of natural killer cells in the generation of influenza virus-specific cytotoxic T cells. Cell Immunol 1996; 173:1; PMID:8871595; http://dx.doi.org/10.1006/cimm.1996.0245
50. + T cells enriched within the gut. Mucosal Immunol 2016; 9:401-13; PMID:26220166; http://dx.doi.org/10.1038/mi.2015.69
51. + T cells defines a distinct functional subset with tissue-homing properties. Proc Natl Acad Sci USA 2010; 107:3006-11; PMID:20133607; http://dx.doi.org/10.1073/pnas.0914839107
52. J.R.Fergusson, V.M.Fleming, P.Klenerman. CD161-expressing human T-cells. Front Immunol 2011; 2:1-7; PMID:22566792; http://dx.doi.org/10.3389/fimmu.2011.00036
53. + T cells suggests a distinct pathway of T cell differentiation. Hepatology 2008; 47:396-406; PMID:18219672; http://dx.doi.org/10.1002/hep.22040
54. + T cells during the evolution of Epstein-Barr virus-specific immune responses in vivo. Viral Immunol 2005; 18:513-22; PMID:16212530; http://dx.doi.org/10.1089/vim.2005.18.513