Selective expansion of merocytic dendritic cells and CD8DCs confers anti-tumour effect of Fms-like tyrosine kinase 3-ligand treatment in vivo

Clinical and Experimental Immunology

Volumn 163, Issue 3, 2011, Pages 381-391

  Hennies, C M ^a   Reboulet, R A ^a   Garcia, Z ^b   Nierkens, S ^c   Wolkers, M C ^d   Janssen, E M ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d SANQUIN RESEARCH   (Netherlands)

Author keywords

Cytotoxic T cell response; Dendritic cell; Tumour; Vaccine

Indexed keywords

CD8 ANTIGEN; DENDRITIC CELL VACCINE; FMS LIKE TYROSINE KINASE 3 LIGAND; LYMPHOCYTE ANTIGEN; OVALBUMIN; TUMOR CELL VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL COUNT; CELL EXPANSION; CELL FUNCTION; CELL POPULATION; DENDRITIC CELL; IMMUNOSTIMULATION; IN VIVO STUDY; MEROCYTIC DENDRITIC CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ADJUVANTS, IMMUNOLOGIC; ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD8; ANTIGENS, SURFACE; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; DENDRITIC CELLS; IMMUNODOMINANT EPITOPES; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NATURAL KILLER T-CELLS; NEOPLASMS; OVALBUMIN; PEPTIDE FRAGMENTS; SPLEEN; SURVIVAL ANALYSIS; VACCINATION;

EID: 79551691247     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2010.04305.x     Document Type: Article

References (69)

1. Aymeric L, Apetoh L, Ghiringhelli F etal. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res 2010; 70:855-8.
2. Palucka K, Ueno H, Zurawski G, Fay J, Banchereau J. Building on dendritic cell subsets to improve cancer vaccines. Curr Opin Immunol 2010; 22:258-63.
3. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007; 449:419-26.
4. Petersen TR, Dickgreber N, Hermans IF. Tumor antigen presentation by dendritic cells. Crit Rev Immunol 2010; 30:345-86.
5. Palucka AK, Ueno H, Fay J, Banchereau J. Dendritic cells: a critical player in cancer therapy? J Immunother 2008; 31:793-805.
6. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol 2000; 164:2978-86.
7. Vremec D, Zorbas M, Scollay R etal. The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J Exp Med 1992; 176:47-58.
8. O'Keeffe M, Hochrein H, Vremec D etal. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 2002; 196:1307-19.
9. Kamath AT, Henri S, Battye F, Tough DF, Shortman K. Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 2002; 100:1734-41.
10. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997; 185:1101-11.
11. Belz GT, Bedoui S, Kupresanin F, Carbone FR, Heath WR. Minimal activation of memory CD8(+) T cell by tissue-derived dendritic cells favors the stimulation of naive CD8(+) T cells. Nat Immunol 2007; 8:1060-6.
12. Janssen E, Tabeta K, Barnes MJ etal. Efficient T cell activation via a Toll-interleukin 1 receptor-independent pathway. Immunity 2006; 24:787-99.
13. Caminschi I, Ahmet F, Heger K etal. Putative IKDCs are functionally and developmentally similar to natural killer cells, but not to dendritic cells. J Exp Med 2007; 204:2579-90.
14. Qiu CH, Miyake Y, Kaise H, Kitamura H, Ohara O, Tanaka M. Novel subset of CD8{alpha}+ dendritic cells localized in the marginal zone is responsible for tolerance to cell-associated antigens. J Immunol 2009; 182:4127-36.
15. Liu K, Nussenzweig MC. Origin and development of dendritic cells. Immunol Rev 2010; 234:45-54.
16. Allan RS, Waithman J, Bedoui S etal. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006; 25:153-62.
17. Belz GT, Shortman K, Bevan MJ, Heath WR. CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J Immunol 2005; 175:196-200.
18. Hoeffel G, Ripoche AC, Matheoud D etal. Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 2007; 27:481-92.
19. Williams CA, Harry RA, McLeod JD. Apoptotic cells induce dendritic cell-mediated suppression via interferon-gamma-induced IDO. Immunology 2008; 124:89-101.
20. Peng YF, Elkon KB. Peripheral CD8 T-cell responses to apoptotic cell proteins and peptides. Crit Rev Immunol 2007; 27:357-65.
21. Ferguson TA, Kazama H. Signals from dying cells: tolerance induction by the dendritic cell. Immunol Res 2005; 32:99-108.
22. Saas P, Bonnefoy F, Kury-Paulin S, Kleinclauss F, Perruche S. Mediators involved in the immunomodulatory effects of apoptotic cells. Transplantation 2007; 84:S31-4.
23. Katz JD, Ondr JK, Opoka RJ, Garcia Z, Janssen EM. Cutting edge: merocytic dendritic cells break T cell tolerance to {beta} cell antigens in nonobese diabetic mouse diabetes. J Immunol 2010; 185:1999-2003.
24. Reboulet R, Hennies CM, Garcia Z, Nierkens S, Janssen EM. Prolonged antigen storage endows merocytic dendritic cells with enhanced capacity to prime anti-tumor responses in tumor-bearing mice. J Immunol 2010; 185:3337-47.
25. Curran MA, Allison JP. Tumor vaccines expressing flt3 ligand synergize with ctla-4 blockade to reject preimplanted tumors. Cancer Res 2009; 69:7747-55.
26. Ramakrishna E, Woller N, Mundt B etal. Antitumoral immune response by recruitment and expansion of dendritic cells in tumors infected with telomerase-dependent oncolytic viruses. Cancer Res 2009; 69:1448-58.
27. King GD, Kroeger KM, Bresee CJ etal. Flt3L in combination with HSV1-TK-mediated gene therapy reverses brain tumor-induced behavioral deficits. Mol Ther 2008; 16:682-90.
28. Chakravarty PK, Guha C, Alfieri A etal. Flt3L therapy following localized tumor irradiation generates long-term protective immune response in metastatic lung cancer: its implication in designing a vaccination strategy. Oncology 2006; 70:245-54.
29. Kutzler MA, Weiner DB. Developing DNA vaccines that call to dendritic cells. J Clin Invest 2004; 114:1241-4.
30. Braun SE, Chen K, Blazar BR etal. Flt3 ligand antitumor activity in a murine breast cancer model: a comparison with granulocyte-macrophage colony-stimulating factor and a potential mechanism of action. Hum Gene Ther 1999; 10:2141-51.
31. Lynch DH, Andreasen A, Maraskovsky E, Whitmore J, Miller RE, Schuh JC. Flt3 ligand induces tumor regression and antitumor immune responses in vivo. Nat Med 1997; 3:625-31.
32. Silver DF, Hempling RE, Piver MS, Repasky EA. Flt-3 ligand inhibits growth of human ovarian tumors engrafted in severe combined immunodeficient mice. Gynecol Oncol 2000; 77:377-82.
33. Brasel K, McKenna HJ, Morrissey PJ etal. Hematologic effects of flt3 ligand in vivo in mice. Blood 1996; 88:2004-12.
34. Maraskovsky E, Brasel K, Teepe M etal. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 1996; 184:1953-62.
35. McKenna HJ, Stocking KL, Miller RE etal. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 2000; 95:3489-97.
36. Schmid MA, Kingston D, Boddupalli S, Manz MG. Instructive cytokine signals in dendritic cell lineage commitment. Immunol Rev 2010; 234:32-44.
37. Ehst BD, Ingulli E, Jenkins MK. Development of a novel transgenic mouse for the study of interactions between CD4 and CD8 T cells during graft rejection. Am J Transplant 2003; 3:1355-62.
38. Lyons AB. Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J Immunol Methods 2000; 243:147-54.
39. Jiang Z, Georgel P, Du X etal. CD14 is required for MyD88-independent LPS signaling. Nat Immunol 2005; 6:565-70.
40. Nikolic-Zugic J, Carbone FR. The effect of mutations in the MHC class I peptide binding groove on the cytotoxic T lymphocyte recognition of the Kb-restricted ovalbumin determinant. Eur J Immunol 1990; 20:2431-7.
41. Benedict CA, Loewendorf A, Garcia Z, Blazar BR, Janssen EM. Dendritic cell programming by cytomegalovirus stunts naive T cell responses via the PD-L1/PD-1 pathway. J Immunol 2008; 180:4836-47.
42. Janssen EM, Lemmens EE, Wolfe T, Christen U, von Herrath MG, Schoenberger SP. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 2003; 421:852-6.
43. McBride S, Hoebe K, Georgel P, Janssen E. Cell-associated double-stranded RNA enhances antitumor activity through the production of type I IFN. J Immunol 2006; 177:6122-8.
44. Colucci F, Di Santo JP. The receptor tyrosine kinase c-kit provides a critical signal for survival, expansion, and maturation of mouse natural killer cells. Blood 2000; 95:984-91.
45. Williams NS, Klem J, Puzanov IJ, Sivakumar PV, Bennett M, Kumar V. Differentiation of NK1.1+, Ly49+ NK cells from flt3+ multipotent marrow progenitor cells. J Immunol 1999; 163:2648-56.
46. Swiecki M, Colonna M. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol Rev 2010; 234:142-62.
47. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001; 106:255-8.
48. Hoebe K, Janssen EM, Kim SO etal. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol 2003; 4:1223-9.
49. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med 1999; 189:521-30.
50. Ogasawara K, Hida S, Weng Y etal. Requirement of the IFN-alpha/beta-induced CXCR3 chemokine signalling for CD8+ T cell activation. Genes Cells 2002; 7:309-20.
51. Le Bon A, Tough DF. Type I interferon as a stimulus for cross-priming. Cytokine Growth Factor Rev 2008; 19:33-40.
52. Shortman K, Heath WR. The CD8+ dendritic cell subset. Immunol Rev 2010; 234:18-31.
53. Kaech SM, Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2001; 2:415-22.
54. Spierings DC, Lemmens EE, Grewal K, Schoenberger SP, Green DR. Duration of CTL activation regulates IL-2 production required for autonomous clonal expansion. Eur J Immunol 2006; 36:1707-17.
55. van Stipdonk MJ, Hardenberg G, Bijker MS etal. Dynamic programming of CD8+ T lymphocyte responses. Nat Immunol 2003; 4:361-5.
56. van Stipdonk MJ, Lemmens EE, Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2001; 2:423-9.
57. Sun JC, Bevan MJ. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science (NY) 2003; 300:339-42.
58. Shedlock DJ, Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science (NY) 2003; 300:337-9.
59. Hamilton-Williams EE, Lang A, Benke D, Davey GM, Wiesmuller KH, Kurts C. Cutting edge: TLR ligands are not sufficient to break cross-tolerance to self-antigens. J Immunol 2005; 174:1159-63.
60. Krawczyk CM, Shen H, Pearce EJ. Memory CD4 T cells enhance primary CD8 T-cell responses. Infect Immun 2007; 75:3556-60.
61. Ryu SJ, Jung KM, Yoo HS etal. Cognate CD4 help is essential for the reactivation and expansion of CD8 memory T cells directed against the hematopoietic cell-specific dominant minor histocompatibility antigen, H60. Blood 2009; 113:4273-80.
62. Novy P, Quigley M, Huang X, Yang Y. CD4 T cells are required for CD8 T cell survival during both primary and memory recall responses. J Immunol 2007; 179:8243-51.
63. Sun JC, Williams MA, Bevan MJ. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 2004; 5:927-33.
64. Bedoui S, Prato S, Mintern J etal. Characterization of an immediate splenic precursor of CD8+ dendritic cells capable of inducing antiviral T cell responses. J Immunol 2009; 182:4200-7.
65. Bachem A, Guttler S, Hartung E etal. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med 2010; 207:1273-81.
66. Crozat K, Guiton R, Contreras V etal. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med 2010; 207:1283-92.
67. Jongbloed SL, Kassianos AJ, McDonald KJ etal. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010; 207:1247-60.
68. Di Pucchio T, Chatterjee B, Smed-Sorensen A etal. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat Immunol 2008; 9:551-7.
69. Mouries J, Moron G, Schlecht G, Escriou N, Dadaglio G, Leclerc C. Plasmacytoid dendritic cells efficiently cross-prime naive T cells in vivo after TLR activation. Blood 2008; 112:3713-22.