CD40-activated B cells induce anti-tumor immunity in vivo

Oncotarget

Volumn 8, Issue 17, 2017, Pages 27740-27753

  Wennhold, Kerstin ^a   Weber, Tanja M ^a   Klein Gonzalez, Nela ^b   Thelen, Martin ^a   Garcia Marquez, Maria ^a   Chakupurakal, Geothy ^a   Fiedler, Anne ^a   Schlösser, Hans A ^a   Fischer, Rieke ^a   Theurich, Sebastian ^a,c   Shimabukuro Vornhagen, Alexander ^a   von Bergwelt Baildon, Michael ^a  

^a UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

Author keywords

Antigen presentation; B cell; Cancer immunotherapy; CD40 activated B cells; Cellular adjuvant

Indexed keywords

TUMOR ANTIGEN; CANCER VACCINE; CD40 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD40 ACTIVATED B CELL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; IN VIVO STUDY; LIMIT OF QUANTITATION; LYMPHOCYTE HOMING; MOUSE; NONHUMAN; TUMOR GROWTH; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DENDRITIC CELL; DRUG SCREENING; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; METABOLISM; NEOPLASM; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

ANIMALS; ANTIGENS, NEOPLASM; B-LYMPHOCYTES; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD40 ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85018390432     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7720     Document Type: Article

References (55)

1. Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, Sharfman WH, Stankevich E, Pons A, Salay TM, McMiller TL, Gilson MM, Wang C, Selby M, Taube JM, Anders R, Chen L, et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol. 2010; 28:3167-3175
2. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010; 363:711-723
3. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012; 366:2443-2454
4. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, Burke MM, Caldwell A, Kronenberg SA, Agunwamba BU, Zhang X, Lowy I, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013; 369:122-133
5. Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT, Gajewski TF. Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Sci Transl Med. 2013; 5:200ra116
6. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, Chen S, Klein AP, Pardoll DM, Topalian SL, Chen L. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012; 4:127ra137
7. Fu J, Malm IJ, Kadayakkara DK, Levitsky H, Pardoll D, Kim YJ. Preclinical evidence that PD1 blockade cooperates with cancer vaccine TEGVAX to elicit regression of established tumors. Cancer Res. 2014; 74:4042-4052
8. Dhodapkar MV, Steinman RM, Sapp M, Desai H, Fossella C, Krasovsky J, Donahoe SM, Dunbar PR, Cerundolo V, Nixon DF, Bhardwaj N. Rapid generation of broad T-cell immunity in humans after a single injection of mature dendritic cells. J Clin Invest. 1999; 104:173-180
9. Draube A, Klein-Gonzalez N, Mattheus S, Brillant C, Hellmich M, Engert A, von Bergwelt-Baildon M. Dendritic cell based tumor vaccination in prostate and renal cell cancer: a systematic review and meta-analysis. PLoS One. 2011; 6:e18801
10. Parkhurst MR, Salgaller ML, Southwood S, Robbins PF, Sette A, Rosenberg SA, Kawakami Y. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J Immunol. 1996; 157:2539-2548
11. Zitvogel L, Mayordomo JI, Tjandrawan T, DeLeo AB, Clarke MR, Lotze MT, Storkus WJ. Therapy of murine tumors with tumor peptide-pulsed dendritic cells: dependence on T cells, B7 costimulation, and T helper cell 1-associated cytokines. The Journal of experimental medicine. 1996; 183:87-97
12. von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol. 2003; 3:867-878
13. Tretter T, Venigalla RK, Eckstein V, Saffrich R, Sertel S, Ho AD, Lorenz HM. Induction of CD4+ T-cell anergy and apoptosis by activated human B cells. Blood. 2008; 112:4555-4564
14. Tu W, Lau YL, Zheng J, Liu Y, Chan PL, Mao H, Dionis K, Schneider P, Lewis DB. Efficient generation of human alloantigen-specific CD4+ regulatory T cells from naive precursors by CD40-activated B cells. Blood. 2008; 112:2554-2562
15. Kleindienst P, Brocker T. Concerted antigen presentation by dendritic cells and B cells is necessary for optimal CD4 T-cell immunity in vivo. Immunology. 2005; 115:556-564
16. Parekh VV, Prasad DV, Banerjee PP, Joshi BN, Kumar A, Mishra GC. B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGF-beta 1. J Immunol. 2003; 170:5897-5911
17. Shimabukuro-Vornhagen A, Kondo E, Liebig T, von Bergwelt-Baildon M. Activated human B cells: stimulatory or tolerogenic antigen-presenting cells? Blood. 2009; 114:746-747; author reply 747
18. Banchereau J, de Paoli P, Valle A, Garcia E, Rousset F. Long-term human B cell lines dependent on interleukin-4 and antibody to CD40. Science. 1991; 251:70-72
19. Schultze JL, Michalak S, Seamon MJ, Dranoff G, Jung K, Daley J, Delgado JC, Gribben JG, Nadler LM. CD40-activated human B cells: An alternative source of highly efficient antigen presenting cells to generate autologous antigen-specific T cells for adoptive immunotherapy. J Clin Invest. 1997; 100:2757-2765
20. von Bergwelt-Baildon MS, Vonderheide RH, Maecker B, Hirano N, Anderson KS, Butler MO, Xia Z, Zeng WY, Wucherpfennig KW, Nadler LM, Schultze JL. Human primary and memory cytotoxic T lymphocyte responses are efficiently induced by means of CD40-activated B cells as antigen-presenting cells: potential for clinical application. Blood. 2002; 99:3319-3325
21. Wiesner M, Zentz C, Mayr C, Wimmer R, Hammerschmidt W, Zeidler R, Moosmann A. Conditional immortalization of human B cells by CD40 ligation. PLoS One. 2008; 3:e1464
22. Lapointe R, Bellemare-Pelletier A, Housseau F, Thibodeau J, Hwu P. CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specific T cells. Cancer Res. 2003; 63:2836-2843
23. Shen S, Xu Z, Qian X, Ding Y, Yu L, Liu B. Autogeneic rna-electroporated CD40-ligand activated b-cells from hepatocellular carcinoma patients induce CD8+ T-cell responses ex vivo. Experimental oncology. 2007; 29:137-143
24. von Bergwelt-Baildon M, Schultze JL, Maecker B, Menezes I, Nadler LM. Correspondence re R. Lapointe et al., CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specific T cells. Cancer Res 2003;63:2836-43. Cancer Res. 2004; 64:4055-4056; author reply 4056-4057
25. Wu C, Liu Y, Zhao Q, Chen GM, Chen JH, Yan XM, Zhou YH, Huang ZH. Soluble CD40 ligand-activated human peripheral B cells as surrogated antigen presenting cells: A preliminary approach for anti-HBV immunotherapy. Virol J. 2010; 7
26. Klein-Gonzalez NK, Wennhold K, Balkow S, Kondo E, Bolck B, Weber T, Garcia-Marquez M, Grabbe S, Bloch W, von Bergwelt-Baildon M, Shimabukuro-VornhagenA. In vitro and in vivo imaging of initial B-T-cell interactions in the setting of B-cell based cancer immunotherapy. Oncoimmunology. 2015; 4:e1038684
27. von Bergwelt-Baildon M, Shimabukuro-Vornhagen A, Popov A, Klein-Gonzalez N, Fiore F, Debey S, Draube A, Maecker B, Menezes I, Nadler LM, Schultze JL. CD40-activated B cells express full lymph node homing triad and induce T-cell chemotaxis: potential as cellular adjuvants. Blood. 2006; 107:2786-2789
28. Li Q, Lao X, Pan Q, Ning N, Yet J, Xu Y, Li S, Chang AE. Adoptive transfer of tumor reactive B cells confers host T-cell immunity and tumor regression. Clin Cancer Res. 2011; 17:4987-4995
29. Mason NJ, Coughlin CM, Overley B, Cohen JN, Mitchell EL, Colligon TA, Clifford CA, Zurbriggen A, Sorenmo KU, Vonderheide RH. RNA-loaded CD40-activated B cells stimulate antigen-specific T-cell responses in dogs with spontaneous lymphoma. Gene therapy. 2008; 15:955-965
30. Sorenmo KU, Krick E, Coughlin CM, Overley B, Gregor TP, Vonderheide RH, Mason NJ. CD40-activated B cell cancer vaccine improves second clinical remission and survival in privately owned dogs with non-Hodgkin's lymphoma. PLoS One. 2011; 6:e24167
31. Garcia-Marquez MA, Shimabukuro-Vornhagen A, Theurich S, Kochanek M, Weber T, Wennhold K, Dauben A, Dzionek A, Reinhard C, von Bergwelt-Baildon M. A multimerized form of recombinant human CD40 ligand supports long-term activation and proliferation of B cells. Cytotherapy. 2014; 16:1537-1544
32. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. The Journal of experimental medicine. 1994; 179:1109-1118
33. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol. 2002; 2:151-161
34. Barrou B, Benoit G, Ouldkaci M, Cussenot O, Salcedo M, Agrawal S, Massicard S, Bercovici N, Ericson ML, Thiounn N. Vaccination of prostatectomized prostate cancer patients in biochemical relapse, with autologous dendritic cells pulsed with recombinant human PSA. Cancer Immunol Immunother. 2004; 53:453-460
35. Berntsen A, Trepiakas R, Wenandy L, Geertsen PF, thor Straten P, Andersen MH, Pedersen AE, Claesson MH, Lorentzen T, Johansen JS, Svane IM. Therapeutic dendritic cell vaccination of patients with metastatic renal cell carcinoma: a clinical phase 1/2 trial. J Immunother. 2008; 31:771-780
36. Fong L, Brockstedt D, Benike C, Wu L, Engleman EG. Dendritic cells injected via different routes induce immunity in cancer patients. J Immunol. 2001; 166:4254-4259
37. Heiser A, Coleman D, Dannull J, Yancey D, Maurice MA, Lallas CD, Dahm P, Niedzwiecki D, Gilboa E, Vieweg J. Autologous dendritic cells transfected with prostate-specific antigen RNA stimulate CTL responses against metastatic prostate tumors. J Clin Invest. 2002; 109:409-417
38. Hildenbrand B, Sauer B, Kalis O, Stoll C, Freudenberg MA, Niedermann G, Giesler JM, Juttner E, Peters JH, Haring B, Leo R, Unger C, Azemar M. Immunotherapy of patients with hormone-refractory prostate carcinoma pre-treated with interferon-gamma and vaccinated with autologous PSA-peptide loaded dendritic cells-a pilot study. The Prostate. 2007; 67:500-508
39. Mu LJ, Kyte JA, Kvalheim G, Aamdal S, Dueland S, Hauser M, Hammerstad H, Waehre H, Raabe N, Gaudernack G. Immunotherapy with allotumour mRNA-transfected dendritic cells in androgen-resistant prostate cancer patients. British journal of cancer. 2005; 93:749-756
40. Schwaab T, Schwarzer A, Wolf B, Crocenzi TS, Seigne JD, Crosby NA, Cole BF, Fisher JL, Uhlenhake JC, Mellinger D, Foster C, Szczepiorkowski ZM, Webber SM, Schned AR, Harris RD, Barth RJ, Jr., et al. Clinical and immunologic effects of intranodal autologous tumor lysatedendritic cell vaccine with Aldesleukin (Interleukin 2) and IFN-(alpha)2a therapy in metastatic renal cell carcinoma patients. Clin Cancer Res. 2009; 15:4986-4992
41. Su Z, Dannull J, Yang BK, Dahm P, Coleman D, Yancey D, Sichi S, Niedzwiecki D, Boczkowski D, Gilboa E, Vieweg J. Telomerase mRNA-transfected dendritic cells stimulate antigen-specific CD8+ and CD4+ T cell responses in patients with metastatic prostate cancer. J Immunol. 2005; 174:3798-3807
42. Waeckerle-Men Y, Uetz-von Allmen E, Fopp M, von Moos R, Bohme C, Schmid HP, Ackermann D, Cerny T, Ludewig B, Groettrup M, Gillessen S. Dendritic cell-based multi-epitope immunotherapy of hormone-refractory prostate carcinoma. Cancer Immunol Immunother. 2006; 55:1524-1533
43. Wei YC, Sticca RP, Li J, Holmes LM, Burgin KE, Jakubchak S, Bouton-Verville H, Williamson J, Meyer K, Evans L, Martin J, Stephenson JJ, Trocha S, Smith S, Wagner TE. Combined treatment of dendritoma vaccine and low-dose interleukin-2 in stage IV renal cell carcinoma patients induced clinical response: A pilot study. Oncol Rep. 2007; 18:665-671
44. Small EJ, Fratesi P, Reese DM, Strang G, Laus R, Peshwa MV, Valone FH. Immunotherapy of hormone-refractory prostate cancer with antigen-loaded dendritic cells. J Clin Oncol. 2000; 18:3894-3903
45. Lee J, Dollins CM, Boczkowski D, Sullenger BA, Nair S. Activated B cells modified by electroporation of multiple mRNAs encoding immune stimulatory molecules are comparable to mature dendritic cells in inducing in vitro antigen-specific T-cell responses. Immunology. 2008; 125:229-240
46. Guo S, Xu J, Denning W, Hel Z. Induction of protective cytotoxic T-cell responses by a B-cell-based cellular vaccine requires stable expression of antigen. Gene therapy. 2009; 16:1300-1313
47. Neron S, Racine C, Roy A, Guerin M. Differential responses of human B-lymphocyte subpopulations to graded levels of CD40-CD154 interaction. Immunology. 2005; 116:454-463
48. Shimabukuro-Vornhagen A, Draube A, Liebig TM, Rothe A, Kochanek M, von Bergwelt-Baildon MS. The immunosuppressive factors IL-10, TGF-beta, and VEGF do not affect the antigen-presenting function of CD40-activated B cells. J Exp Clin Cancer Res. 2012; 31:47
49. Opal SM. Endotoxins and other sepsis triggers. Contributions to nephrology. 2010; 167:14-24
50. Rodriguez-Pinto D, Moreno J. B cells can prime naive CD4+ T cells in vivo in the absence of other professional antigen-presenting cells in a CD154-CD40-dependent manner. Eur J Immunol. 2005; 35:1097-1105
51. Batista FD, Neuberger MS. Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity. 1998; 8:751-759
52. Tasian SK, Gardner RA. CD19-redirected chimeric antigen receptor-modified T cells: a promising immunotherapy for children and adults with B-cell acute lymphoblastic leukemia (ALL). Therapeutic advances in hematology. 2015; 6:228-241
53. Gurcan HM, Keskin DB, Stern JN, Nitzberg MA, Shekhani H, Ahmed AR. A review of the current use of rituximab in autoimmune diseases. International immunopharmacology. 2009; 9:10-25
54. Blank C, Brown I, Peterson AC, Spiotto M, Iwai Y, Honjo T, Gajewski TF. PD-L1/B7H-1 inhibits the effector phase of tumor rejection by T cell receptor (TCR) transgenic CD8+ T cells. Cancer Res. 2004; 64:1140-1145
55. Liebig TM, Fiedler A, Klein-Gonzalez N, Shimabukuro-Vornhagen A, von Bergwelt-Baildon M. Murine model of CD40-activation of B cells. J Vis Exp. 2010; doi: 10.3791/1734