Revisiting the prominent anti-tumoral potential of pre-mNK cells

Frontiers in Immunology

Volumn 4, Issue DEC, 2013, Pages

  Guimont Desrochers, Fanny ^a,b   Lesage, Sylvie ^a,b  

^a MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Anti tumoral activity; Cellular differentiation; Human; Mouse; Natural killer cells; Pre mNK cells

Indexed keywords

EID: 84892168819     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00446     Document Type: Review

References (66)

1. Kiessling R, Klein E, Pross H, Wigzell H. "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol (1975) 5:117-21. doi:10.1002/eji.1830050208.
2. Trinchieri G. Biology of natural killer cells. Adv Immunol (1989) 47:187-376.
3. Walzer T, Dalod M, Vivier E, Zitvogel L. Natural killer cell-dendritic cell crosstalk in the initiation of immune responses. Expert Opin Biol Ther (2005) 5(Suppl 1):S49-59. doi:10.1517/14712598.5.1.S49.
4. Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol (2007) 7:19-30. doi:10.1038/nri1996.
5. Spits H, Lanier LL. Natural killer or dendritic: what's in a name? Immunity (2007) 26:11-6. doi:10.1016/j.immuni.2007.01.004.
6. Ullrich E, Chaput N, Zitvogel L. Killer dendritic cells and their potential role in immunotherapy. Horm Metab Res (2008) 40:75-81. doi:10.1055/s-2007-1022554.
7. Phillips JH, Le AM, Lanier LL. Natural killer cells activated in a human mixed lymphocyte response culture identified by expression of Leu-11 and class II histocompatibility antigens. J Exp Med (1984) 159:993-1008. doi:10.1084/jem.159.4.993.
8. Roncarolo MG, Bigler M, Haanen JB, Yssel H, Bacchetta R, De Vries JE, et al. Natural killer cell clones can efficiently process and present protein antigens. J Immunol (1991) 147:781-7.
9. Hanna J, Gonen-Gross T, Fitchett J, Rowe T, Daniels M, Arnon TI, et al. Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest (2004) 114:1612-23. doi:10.1172/JCI22787.
10. Zingoni A, Sornasse T, Cocks BG, Tanaka Y, Santoni A, Lanier LL. Cross-talk between activated human NK cells and CD4+ T cells via OX40-OX40 ligand interactions. J Immunol (2004) 173:3716-24.
11. Josien R, Heslan M, Soulillou JP, Cuturi MC. Rat spleen dendritic cells express natural killer cell receptor protein 1 (NKR-P1) and have cytotoxic activity to select targets via a Ca2+-dependent mechanism. J Exp Med (1997) 186:467-72. doi:10.1084/jem.186.3.467.
12. Fanger NA, Maliszewski CR, Schooley K, Griffith TS. Human dendritic cells mediate cellular apoptosis via tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J Exp Med (1999) 190:1155-64. doi:10.1084/jem.190.8.1155.
13. Chapoval AI, Tamada K, Chen L. In vitro growth inhibition of a broad spectrum of tumor cell lines by activated human dendritic cells. Blood (2000) 95:2346-51.
14. Trinite B, Voisine C, Yagita H, Josien R. A subset of cytolytic dendritic cells in rat. J Immunol (2000) 165:4202-8.
15. Janjic BM, Lu G, Pimenov A, Whiteside TL, Storkus WJ, Vujanovic NL. Innate direct anticancer effector function of human immature dendritic cells. I. Involvement of an apoptosis-inducing pathway. J Immunol (2002) 168:1823-30.
16. Lu G, Janjic BM, Janjic J, Whiteside TL, Storkus WJ, Vujanovic NL. Innate direct anticancer effector function of human immature dendritic cells. II. Role of TNF, lymphotoxin-alpha(1)beta(2), Fas ligand, and TNF-related apoptosis-inducing ligand. J Immunol (2002) 168:1831-9.
17. Trinite B, Chauvin C, Peche H, Voisine C, Heslan M, Josien R. Immature CD4- CD103+ rat dendritic cells induce rapid caspase-independent apoptosis-like cell death in various tumor and nontumor cells and phagocytose their victims. J Immunol (2005) 175:2408-17.
18. Srivastava RM, Varalakshmi C, Khar A. Cross-linking a mAb to NKR-P2/NKG2D on dendritic cells induces their activation and maturation leading to enhanced anti-tumor immune response. Int Immunol (2007) 19:591-607. doi:10.1093/intimm/dxm024.
19. Tel J, Smits EL, Anguille S, Joshi RN, Figdor CG, De Vries IJ. Human plasmacytoid dendritic cells are equipped with antigen-presenting and tumoricidal capacities. Blood (2012) 120:3936-44. doi:10.1182/blood-2012-06-435941.
20. Strioga M, Schijns V, Powell DJ Jr, Pasukoniene V, Dobrovolskiene N, Michalek J. Dendritic cells and their role in tumor immunosurveillance. Innate Immun (2013) 19:98-111. doi:10.1177/1753425912449549.
21. Chan CW, Crafton E, Fan HN, Flook J, Yoshimura K, Skarica M, et al. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat Med (2006) 12:207-13. doi:10.1038/nm1352.
22. Taieb J, Chaput N, Menard C, Apetoh L, Ullrich E, Bonmort M, et al. A novel dendritic cell subset involved in tumor immunosurveillance. Nat Med (2006) 12:214-9. doi:10.1038/nm1356.
23. Himoudi N, Nabarro S, Buddle J, Eddaoudi A, Thrasher AJ, Anderson J. Bone marrow-derived IFN-producing killer dendritic cells account for the tumoricidal activity of unpulsed dendritic cells. J Immunol (2008) 181:6654-63.
24. Jiang Q, Wei H, Tian Z. IFN-producing killer dendritic cells contribute to the inhibitory effect of poly I:C on the progression of murine melanoma. J Immunother (2008) 31:555-62. doi:10.1097/CJI.0b013e31817d8e75.
25. Shortman K, Villadangos JA. Is it a DC, is it an NK? No, it's an IKDC. Nat Med (2006) 12:167-8. doi:10.1038/nm0206-167.
26. Blasius AL, Barchet W, Cella M, Colonna M. Development and function of murine B220+CD11c+NK1.1+ cells identify them as a subset of NK cells. J Exp Med (2007) 204:2561-8. doi:10.1084/jem.20070991.
27. Caminschi I, Ahmet F, Heger K, Brady J, Nutt SL, Vremec D, et al. Putative IKDCs are functionally and developmentally similar to natural killer cells, but not to dendritic cells. J Exp Med (2007) 204:2579-90. doi:10.1084/jem.20071351.
28. Vosshenrich CA, Lesjean-Pottier S, Hasan M, Richard-Le Goff O, Corcuff E, Mandelboim O, et al. CD11cloB220+ interferon-producing killer dendritic cells are activated natural killer cells. J Exp Med (2007) 204:2569-78. doi:10.1084/jem.20071451.
29. GeurtsvanKessel CH, Bergen IM, Muskens F, Boon L, Hoogsteden HC, Osterhaus AD, et al. Both conventional and interferon killer dendritic cells have antigen-presenting capacity during influenza virus infection. PLoS One (2009) 4:e7187. doi:10.1371/journal.pone.0007187.
30. Guimont-Desrochers F, Boucher G, Dong Z, Dupuis M, Veillette A, Lesage S. Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation. Blood (2012) 119:4349-57. doi:10.1182/blood-2011-11-395954.
31. Zitvogel L, Housseau F. IKDCs or B220+ NK cells are pre-mNK cells. Blood (2012) 119:4345-6. doi:10.1182/blood-2012-03-415026.
32. Chaput N, Flament C, Locher C, Desbois M, Rey A, Rusakiewicz S, et al. Phase I clinical trial combining imatinib mesylate and IL-2: HLA-DR NK cell levels correlate with disease outcome. Oncoimmunology (2013) 2:e23080. doi:10.4161/onci.23080.
33. Nakano H, Yanagita M, Gunn MD. CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med (2001) 194:1171-8. doi:10.1084/jem.194.8.1171.
34. Welner RS, Pelayo R, Garrett KP, Chen X, Perry SS, Sun XH, et al. Interferon-producing killer dendritic cells (IKDCs) arise via a unique differentiation pathway from primitive c-kitHiCD62L+ lymphoid progenitors. Blood (2007) 109:4825-931. doi:10.1182/blood-2006-08-043810.
35. Wu L, Liu YJ. Development of dendritic-cell lineages. Immunity (2007) 26:741-50. doi:10.1016/j.immuni.2007.06.006.
36. Ullrich E, Bonmort M, Mignot G, Jacobs B, Bosisio D, Sozzani S, et al. Trans-presentation of IL-15 dictates IFN-producing killer dendritic cells effector functions. J Immunol (2008) 180:7887-97.
37. Moretta A, Poggi A, Pende D, Tripodi G, Orengo AM, Pella N, et al. CD69-mediated pathway of lymphocyte activation: anti-CD69 monoclonal antibodies trigger the cytolytic activity of different lymphoid effector cells with the exception of cytolytic T lymphocytes expressing T cell receptor alpha/beta. J Exp Med (1991) 174:1393-8. doi:10.1084/jem.174.6.1393.
38. Montel AH, Bochan MR, Hobbs JA, Lynch DH, Brahmi Z. Fas involvement in cytotoxicity mediated by human NK cells. Cell Immunol (1995) 166:236-46. doi:10.1006/cimm.1995.9974.
39. Sague SL, Tato C, Pure E, Hunter CA. The regulation and activation of CD44 by natural killer (NK) cells and its role in the production of IFN-gamma. J Interferon Cytokine Res (2004) 24:301-9. doi:10.1089/107999004323065093.
40. Nakayama M, Takeda K, Kawano M, Takai T, Ishii N, Ogasawara K. Natural killer (NK)-dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4+ T cells. Proc Natl Acad Sci U S A (2011) 108:18360-5. doi:10.1073/pnas.1110584108.
41. Huntington ND, Vosshenrich CA, Di Santo JP. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat Rev Immunol (2007) 7:703-14. doi:10.1038/nri2154.
42. Milush JM, Long BR, Snyder-Cappione JE, Cappione AJ III, York VA, Ndhlovu LC, et al. Functionally distinct subsets of human NK cells and monocyte/DC-like cells identified by coexpression of CD56, CD7, and CD4. Blood (2009) 114:4823-31. doi:10.1182/blood-2009-04-216374.
43. Evans JH, Horowitz A, Mehrabi M, Wise EL, Pease JE, Riley EM, et al. A distinct subset of human NK cells expressing HLA-DR expand in response to IL-2 and can aid immune responses to BCG. Eur J Immunol (2011) 41:1924-33. doi:10.1002/eji.201041180.
44. Arina A, Murillo O, Dubrot J, Azpilikueta A, Gabari I, Perez-Gracia JL, et al. Interleukin-15 liver gene transfer increases the number and function of IKDCs and NK cells. Gene Ther (2008) 15:473-83. doi:10.1038/gt.2008.4.
45. Rolink A, Ten Boekel E, Melchers F, Fearon DT, Krop I, Andersson J. A subpopulation of B220+ cells in murine bone marrow does not express CD19 and contains natural killer cell progenitors. J Exp Med (1996) 183:187-94. doi:10.1084/jem.183.1.187.
46. Fathman JW, Bhattacharya D, Inlay MA, Seita J, Karsunky H, Weissman IL. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood (2011) 118:5439-47. doi:10.1182/blood-2011-04-348912.
47. Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood (2009) 113:5488-96. doi:10.1182/blood-2008-10-187179.
48. Yamada H, Kishihara K, Kong YY, Nomoto K. Enhanced generation of NK cells with intact cytotoxic function in CD45 exon 6-deficient mice. J Immunol (1996) 157:1523-8.
49. Huntington ND, Xu Y, Nutt SL, Tarlinton DM. A requirement for CD45 distinguishes Ly49D-mediated cytokine and chemokine production from killing in primary natural killer cells. J Exp Med (2005) 201:1421-33. doi:10.1084/jem.20042294.
50. Hesslein DG, Takaki R, Hermiston ML, Weiss A, Lanier LL. Dysregulation of signaling pathways in CD45-deficient NK cells leads to differentially regulated cytotoxicity and cytokine production. Proc Natl Acad Sci U S A (2006) 103:7012-7. doi:10.1073/pnas.0601851103.
51. Vosshenrich CA, Garcia-Ojeda ME, Samson-Villeger SI, Pasqualetto V, Enault L, Richard-Le Goff O, et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol (2006) 7:1217-24. doi:10.1038/ni1395.
52. Luther C, Warner K, Takei F. Unique progenitors in mouse lymph node develop into CD127+ NK cells: thymus-dependent and thymus-independent pathways. Blood (2011) 117:4012-21. doi:10.1182/blood-2010-07-298901.
53. Pautier P, Locher C, Robert C, Deroussent A, Flament C, Le Cesne A, et al. Phase I clinical trial combining imatinib mesylate and IL-2 in refractory cancer patients: IL-2 interferes with the pharmacokinetics of imatinib mesylate. Oncoimmunology (2013) 2:e23079. doi:10.4161/onci.23079.
54. Vremec D, O'Keeffe M, Hochrein H, Fuchsberger M, Caminschi I, Lahoud M, et al. Production of interferons by dendritic cells, plasmacytoid cells, natural killer cells, and interferon-producing killer dendritic cells. Blood (2007) 109:1165-73. doi:10.1182/blood-2006-05-015354.
55. Mignot G, Ullrich E, Bonmort M, Menard C, Apetoh L, Taieb J, et al. The critical role of IL-15 in the antitumor effects mediated by the combination therapy imatinib and IL-2. J Immunol (2008) 180:6477-83.
56. Terme M, Mignot G, Ullrich E, Bonmort M, Minard-Colin V, Jacquet A, et al. The dendritic cell-like functions of IFN-producing killer dendritic cells reside in the CD11b+ subset and are licensed by tumor cells. Cancer Res (2009) 69:6590-7. doi:10.1158/0008-5472.CAN-08-4473.
57. Sandau MM, Schluns KS, Lefrancois L, Jameson SC. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15R alpha by the same cells. J Immunol (2004) 173:6537-41.
58. Do JS, Min B. IL-15 produced and trans-presented by DCs underlies homeostatic competition between CD8 and {gamma}{delta} T cells in vivo. Blood (2009) 113:6361-71. doi:10.1182/blood-2008-12-192997.
59. Himoudi N, Yan M, Bouma G, Morgenstern D, Wallace R, Seddon B, et al. Migratory and antigen presentation functions of IFN-producing killer dendritic cells. Cancer Res (2009) 69:6598-606. doi:10.1158/0008-5472.CAN-09-0501.
60. Hardy AW, Graham DR, Shearer GM, Herbeuval JP. HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIV coreceptors by Toll-like receptor 7-induced IFN-alpha. Proc Natl Acad Sci U S A (2007) 104:17453-8. doi:10.1073/pnas.0707244104.
61. Pletneva M, Fan H, Park JJ, Radojcic V, Jie C, Yu Y, et al. IFN-producing killer dendritic cells are antigen-presenting cells endowed with T-cell cross-priming capacity. Cancer Res (2009) 69:6607-14. doi:10.1158/0008-5472.CAN-09-0508.
62. Homann D, Jahreis A, Wolfe T, Hughes A, Coon B, Van Stipdonk MJ, et al. CD40L blockade prevents autoimmune diabetes by induction of bitypic NK/DC regulatory cells. Immunity (2002) 16:403-15. doi:10.1016/S1074-7613(02)00290-X.
63. Guimont-Desrochers F, Cappello ZJ, Chagnon M, McDuffie M, Lesage S. Cutting edge: genetic characterization of IFN-producing killer dendritic cells. J Immunol (2009) 182:5193-7. doi:10.4049/jimmunol.0803969.
64. McDuffie M. Derivation of diabetes-resistant congenic lines from the nonobese diabetic mouse. Clin Immunol (2000) 96:119-30. doi:10.1006/clim.2000.4893.
65. Chen J, Reifsnyder PC, Scheuplein F, Schott WH, Mileikovsky M, Soodeen-Karamath S, et al. "Agouti NOD": identification of a CBA-derived IDD locus on chromosome 7 and its use for chimera production with NOD embryonic stem cells. Mamm Genome (2005) 16:775-83. doi:10.1007/s00335-005-0007-1.
66. Huarte E, Rynda-Apple A, Riccardi C, Skyberg JA, Golden S, Rollins MF, et al. Tolerogen-induced interferon-producing killer dendritic cells (IKDCs) protect against EAE. J Autoimmun (2011) 37:328-41. doi:10.1016/j.jaut.2011.09.005.