Apoptotic blebs from leukemic cells as a preferred source of tumor-associated antigen for dendritic cell-based vaccines

Cancer Immunology, Immunotherapy

Volumn 63, Issue 4, 2014, Pages 335-345

  Ruben, Jurjen M ^a   Van Den Ancker, Willemijn ^a   Bontkes, Hetty J ^a   Westers, Theresia M ^a   Hooijberg, Erik ^a   Ossenkoppele, Gert J ^a   De Gruijl, Tanja D ^a   Van De Loosdrecht, Arjan A ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Anti tumor immunity; Apoptotic tumor cells; Blebs; Dendritic cell loading; Dendritic cell vaccination; T cell priming

Indexed keywords

DENDRITIC CELL VACCINE; EPITOPE; LEUKEMIA ANTIGEN;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; APOPTOTIC BLEB; ARTICLE; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL FRACTIONATION; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL ORGANELLE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HEAT SHOCK; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; LEUKEMIA CELL LINE; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; APOPTOSIS; CANCER VACCINES; CELL MOVEMENT; CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; DENDRITIC CELLS; HL-60 CELLS; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA RELEASE TESTS; LEUKEMIA, PROMYELOCYTIC, ACUTE; LYMPHOCYTE CULTURE TEST, MIXED; MITOXANTRONE; MONOCYTES; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84896489302     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1515-6     Document Type: Article

References (41)

1. Banchereau J, Palucka K (2005) Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol 5:296-306. doi:10.1038/nri1592 (Pubitemid 40516155)
2. Steinman RM, Banchereau J (2007) Taking dendritic cells into medicine. Nature 449:419-426. doi:10.1038/nature06175 (Pubitemid 47509552)
3. Westers TM, Stam AGM, Scheper RJ et al (2003) Rapid generation of antigen-presenting cells from leukaemic blasts in acute myeloid leukaemia. Cancer Immunol Immunother 52:17-27. doi:10.1007/s00262-002-0316-0 (Pubitemid 36177222)
4. Westers TM, Van Den Ancker W, Bontkes HJ et al (2011) Chronic myeloid leukemia lysate-loaded dendritic cells induce T-cell responses towards leukemia progenitor cells. Immunotherapy 3:569-576
5. Nestle FO, Alijagic S, Gilliet M et al (1998) Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med 4:328-332 (Pubitemid 28144092)
6. Thurner B, Haendle I, Röder C et al (1999) Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J Exp Med 190:1669-1678 (Pubitemid 30002348)
7. Van Tendeloo VF, Van de Velde A, Van Driessche A et al (2010) Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci USA 107:13824-13829. doi:10.1073/pnas.1008051107
8. Boczkowski D, Nair SK, Snyder D, Gilboa E (1996) Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med 184:465-472 (Pubitemid 26324100)
9. Bontkes HJ, Kramer D, Ruizendaal JJ et al (2007) Dendritic cells transfected with interleukin-12 and tumor-associated antigen messenger RNA induce high avidity cytotoxic T cells. Gene Ther 14:366-375 (Pubitemid 46231930)
10. Willemijn VDA, Van Luijn MM, Westers TM et al (2010) Recent advances in antigen-loaded dendritic cell-based strategies for treatment of minimal residual disease in acute myeloid leukemia. Immunotherapy 2:69-83
11. Van den Ancker W, van Luijn MM, Ruben JM et al (2011) Targeting Toll-like receptor 7/8 enhances uptake of apoptotic leukemic cells by monocyte-derived dendritic cells but interferes with subsequent cytokine-induced maturation. Cancer Immunol Immunother 60:37-47. doi:10.1007/s00262-010-0917-y
12. Kitawaki T, Kadowaki N, Fukunaga K et al (2011) Cross-priming of CD8(+) T cells in vivo by dendritic cells pulsed with autologous apoptotic leukemic cells in immunotherapy for elderly patients with acute myeloid leukemia. Exp Hematol 39(424-433):e2. doi:10.1016/j.exphem.2011.01.001
13. Liu K, Iyoda T, Saternus M et al (2002) Immune tolerance after delivery of dying cells to dendritic cells in situ. J Exp Med 196:1091-1097. doi:10.1084/jem.20021215 (Pubitemid 35231767)
14. Morelli AE (2006) The immune regulatory effect of apoptotic cells and exosomes on dendritic cells: its impact on transplantation. Am J Transplant 6:254-261. doi:10.1111/j.1600-6143.2005.01197.x
15. Municio C, Hugo E, Alvarez Y et al (2011) Apoptotic cells enhance IL-10 and reduce IL-23 production in human dendritic cells treated with zymosan. Mol Immunol 1-10. doi:10.1016/j.molimm.2011.07.022
16. Ren G, Su J, Zhao X et al (2008) Apoptotic cells induce immunosuppression through dendritic cells: critical roles of IFN-gamma and nitric oxide. J Immunol 181:3277-3284
17. Sen P, Wallet MA, Yi Z et al (2007) Apoptotic cells induce Mer tyrosine kinase-dependent blockade of NF-κB activation in dendritic cells. Blood 109:653-660. doi:10.1182/blood-2006-04-017368 (Pubitemid 46105966)
18. Stuart LM, Lucas M, Simpson C et al (2002) Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol 168:1627-1635 (Pubitemid 34135757)
19. Lomonosova E, Chinnadurai G (2008) BH3-only proteins in apoptosis and beyond: an overview. Oncogene 27(Suppl 1):S2-S19
20. Franz S, Herrmann K, Fürnrohr BG et al (2007) After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ 14:733-742. doi:10.1038/sj.cdd.4402066 (Pubitemid 46444511)
21. Lane JD, Allan VJ, Woodman PG (2005) Active relocation of chromatin and endoplasmic reticulum into blebs in late apoptotic cells. J Cell Sci 118:4059-4071. doi:10.1242/jcs.02529 (Pubitemid 41410287)
22. Meesmann HM, Fehr E-M, Kierschke S et al (2010) Decrease of sialic acid residues as an eat-me signal on the surface of apoptotic lymphocytes. J Cell Sci 123:3347-3356
23. Fransen JH, Hilbrands LB, Ruben J et al (2009) Mouse dendritic cells matured by ingestion of apoptotic blebs induce T cells to produce interleukin-17. Arthritis Rheum 60:2304-2313. doi:10.1002/art.24719
24. Suber T, Rosen A (2009) Apoptotic cell blebs: repositories of autoantigens and contributors to immune context. Arthritis Rheum 60:2216-2219. doi:10.1002/art.24715
25. Wlodkowic D, Skommer J, Pelkonen J (2007) Towards an understanding of apoptosis detection by SYTO dyes. Cytom Part A J Int Soc Anal Cytol 71:61-72. doi: 10.1002/cyto.a.20366
26. Liu Y, Qureshi M, Xiang J (2002) Antitumor immune responses derived from transgenic expression of CD40 ligand in myeloma cells. Cancer Biother Radiopharm 17:11-18. doi:10.1089/10849780252824028 (Pubitemid 34208167)
27. Schreurs MWJ, Scholten KBJ, Kueter EWM et al (2003) In vitro generation and life span extension of human papillomavirus type 16-specific, healthy donor-derived CTL clones. J Immunol 171:2912-2921 (Pubitemid 37093512)
28. Hooijberg E, Ruizendaal JJ, Snijders PJ et al (2000) Immortalization of human CD8+ T cell clones by ectopic expression of telomerase reverse transcriptase. J Immunol 165:4239-4245
29. Mathivanan S, Ji H, Simpson RJ (2010) Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73:1907-1920. doi:10.1016/j.jprot.2010.06.006
30. Fischer E, Kobold S, Kleber S et al (2010) Cryptic epitopes induce high-titer humoral immune response in patients with cancer. J Immunol 185:3095-3102
31. Fransen JH, Hilbrands LB, Jacobs CW et al (2009) Both early and late apoptotic blebs are taken up by DC and induce IL-6 production. Autoimmunity 42:325-327
32. Verdijk P, Aarntzen EHJG, Lesterhuis WJ et al (2009) Limited amounts of dendritic cells migrate into the T-cell area of lymph nodes but have high immune activating potential in melanoma patients. Clin Cancer Res 15:2531-2540. doi:10.1158/1078-0432.CCR-08-2729
33. Wickman GR, Julian L, Mardilovich K et al (2013) Blebs produced by actin-myosin contraction during apoptosis release damage-associated molecular pattern proteins before secondary necrosis occurs. Cell Death Differ. doi:10.1038/cdd.2013.69
34. Gallucci S, Lolkema M, Matzinger P (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5:1249-1255. doi:10.1038/15200 (Pubitemid 29535601)
35. Herr W, Ranieri E, Olson W et al (2000) Mature dendritic cells pulsed with freeze-thaw cell lysates define an effective in vitro vaccine designed to elicit EBV-specific CD4(+) and CD8 (+) T lymphocyte responses. Blood 96:1857-1864 (Pubitemid 30661071)
36. Schnurr M, Galambos P, Scholz C et al (2001) Tumor cell lysate-pulsed human dendritic cells induce a T-cell response against pancreatic carcinoma cells: an in vitro model for the assessment of tumor vaccines. Cancer Res 61(17):6445-6450 (Pubitemid 32783250)
37. Kokhaei P, Rezvany MR, Virving L et al (2003) Dendritic cells loaded with apoptotic tumour cells induce a stronger T-cell response than dendritic cell-tumour hybrids in B-CLL. Leukemia 17:894-899. doi:10.1038/sj.leu.2402913 (Pubitemid 36626317)
38. Wieckowski E, Chatta GS, Mailliard RM et al (2011) Type-1 polarized dendritic cells loaded with apoptotic prostate cancer cells are potent inducers of CD8(+) T cells against prostate cancer cells and defined prostate cancer-specific epitopes. Prostate 71:125-133. doi:10.1002/pros.21228
39. Dolan BP, Li L, Takeda K et al (2010) Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase. J Immunol 184:1419-1424
40. Yewdell JW, Nicchitta CV (2006) The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol 27:368-373. doi:10.1016/j.it.2006.06.008 (Pubitemid 44038666)
41. Li Y, Wang L-X, Pang P et al (2011) Tumor-derived autophagosome vaccine: mechanism of cross-presentation and therapeutic efficacy. Clin Cancer Res 17:7047-7057. doi:10.1158/1078-0432.CCR-11-0951