Generation of a novel regulatory NK cell subset from peripheral blood CD34+ progenitors promoted by membrane-bound IL-15

PLoS ONE

Volumn 3, Issue 5, 2008, Pages

  Giuliani, Massimo ^a,b   Giron Michel, Julien ^a,b   Negrini, Simone ^a,c   Vacca, Paola ^b,c,d   Durali, Deniz ^a   Caignard, Anne ^e   Le Bousse Kerdiles, Caroline ^a   Chouaib, Salem ^e   Devocelle, Aurore ^a   Bahri, Rajia ^a   Durrbach, Antoine ^a   Taoufik, Yassine ^a   Ferrini, Silvano ^d   Croce, Michela ^d   Mingari, Maria Cristina ^c,d   Moretta, Lorenzo ^b   Azzarone, Bruno ^a  

^a INSERM   (France)

^b G GASLINI INSTITUTE   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD34 ANTIGEN; CD56 ANTIGEN; CD69 ANTIGEN; CD94 ANTIGEN; CHEMOKINE RECEPTOR CCR7; HLA G ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 15; INTERLEUKIN 21; PROTEIN P30; PROTEIN P46; STAT6 PROTEIN; TRANSCRIPTION FACTOR GATA 3;

ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNE DISEASE; BIOLOGICAL THERAPY; BONE MARROW CELL; CD34 SELECTION; CELL CONTACT; CELL CULTURE; CELL ISOLATION; CELL KILLING; CELL MATURATION; CELL STRAIN HL 60; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; CYTOTOXIC LYMPHOCYTE; DENDRITIC CELL; DOWN REGULATION; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; MEDICAL RESEARCH; MEMBRANE BINDING; NATURAL KILLER CELL; ORGAN TRANSPLANTATION; PERIPHERAL BLOOD STEM CELL; PHENOTYPE; CELL MEMBRANE; CLASSIFICATION; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE SUBPOPULATION; METABOLISM; PHYSIOLOGY; STEM CELL; TUMOR CELL LINE;

ANTIGENS, CD34; CELL LINE, TUMOR; CELL MEMBRANE; HUMANS; INTERLEUKIN-15; KILLER CELLS, NATURAL; LYMPHOCYTE SUBSETS; STEM CELLS;

EID: 48249140243     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002241     Document Type: Article

References (60)

1. Cooper MA, Fehniger TA, Fuchs A, Colonna M, Caligiuri MA (2004) NK cell and DC interactions. Trends Immunol 25: 47-52.
2. Li Z, Lim WK, Mahesh SP, Liu B, Nussenblatt RB (2005) Cutting edge: in vivo blockade of human IL-2 receptor induces expansion of CD56(bright) regulatory NK cells in patients with active uveitis. J Immunol 174: 5187-5191.
3. Marcenaro E, Dondero A, Moretta A (2006) Multi-directional cross-regulation of NK cell function during innate immune responses. Transpl Immunol 17: 16-19.
4. Spits H, Lanier LL (2007) Natural killer or dendritic: what's in a name? Immunity 26: 11-16.
5. Zhang C, Zhang J, Tian Z (2006) The regulatory effect of natural killer cells: do "NK-reg cells" exist? Cell Mol Immunol 3: 241-254.
6. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, et al. (2000) Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191: 771-780.
7. Lodolce JP, Boone DL, Chai S, Swain RE, Dassopoulos T, et al. (1998) IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9: 669-676.
8. Giri JG, Ahdieh M, Eisenman J, Shanebeck K, Grabstein K, et al. (1994) Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15. Embo J 13: 2822-2830.
9. Grabstein KH, Eisenman J, Shanebeck K, Rauch C, Srinivasan S, et al. (1994) Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science 264: 965-968.
10. Budagian V, Bulanova E, Orinska Z, Pohl T, Borden EC, et al. (2004) Reverse signaling through membrane-bound interleukin-15. J Biol Chem 279: 42192-42201.
11. Dubois S, Mariner J, Waldmann TA, Tagaya Y (2002) IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 17: 537-547.
12. Giron-Michel J, Giuliani M, Fogli M, Brouty-Boye D, Ferrini S, et al. (2005) Membrane-bound and soluble IL-15/IL-15Ralpha complexes display differential signaling and functions on human hematopoietic progenitors. Blood 106: 2302-2310.
13. Burkett PR, Koka R, Chien M, Chai S, Boone DL, et al. (2004) Coordinate expression and trans presentation of interleukin (IL)-15Ralpha and IL-15 supports natural killer cell and memory CD8+ T cell homeostasis. J Exp Med 200: 825-834.
14. Schluns KS, Nowak EC, Cabrera-Hernandez A, Puddington L, Lefrancois L, et al. (2004) Distinct cell types control lymphoid subset development by means of IL-15 and IL-15 receptor alpha expression. Proc Natl Acad Sci U S A 101: 5616-5621.
15. Briard D, Brouty-Boye D, Azzarone B, Jasmin C (2002) Fibroblasts from human spleen regulate NK cell differentiation from blood CD34(+) progenitors via cell surface IL-15. J Immunol 168: 1326-4332.
16. Briard D, Azzarone B, Brouty-Boye D (2005) Importance of stromal determinants in the generation of dendritic and natural killer cells in the human spleen. Clin Exp Immunol 140: 265-273.
17. Colucci F, Caligiuri MA, Di Santo JP (2003) What does it take to make a natural killer? Nat Rev Immunol 3: 413-425.
18. Yu H, Fehniger TA, Fuchshuber P, Thiel KS, Vivier E, et al. (1998) Flt3 ligand promotes the generation of a distinct CD34(+) human natural killer cell progenitor that responds to interleukin-15. Blood 92: 3647-3657.
19. LeMaoult J, Zafaranloo K, Le Danff C, Carosella ED (2005) HLA-G upregulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. Faseb J 19: 662-664.
20. Giron-Michel J, Caignard A, Fogli M, Brouty-Boye D, Briard D, et al. (2003) Differential STAT3, STAT5, and NF-kappaB activation in human hematopoietic progenitors by endogenous interleukin-15: implications in the expression of functional molecules. Blood 102: 109-117.
21. Ghiringhelli F, Menard C, Terme M, Flament C, Taieb J, et al. (2005) CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 202: 1075-1085.
22. Alvarado J, Taylor P, Castillo JR, Thomas LE (2005) Interferon gamma bound to extracellular matrix changes the hyporesponsiveness to LPS in crypt but not villous intestinal epithelial cells. Immunol Lett 99: 109-112.
23. Capsoni F, Minonzio F, Mariani C, Ongari AM, Bonara P, et al. (1998) Development of phagocytic function of cultured human monocytes is regulated by cell surface IL-10. Cell Immunol 189: 51-59.
24. Carayol G, Robin C, Bourhis JH, Bennaceur-Griscelli A, Chouaib S, et al. (1998) NK cells differentiated from bone marrow, cord blood and peripheral blood stem cells exhibit similar phenotype and functions. Eur J Immunol 28: 1991-2002.
25. Kuwajima S, Sato T, Ishida K, Tada H, Tezuka H, et al. (2006) Interleukin 15-dependent crosstalk between conventional and plasmacytoid dendritic cells is essential for CpG-induced immune activation. Nat Immunol 7: 740-746.
26. Trinder P, Seitzer U, Gerdes J, Seliger B, Macurer M (1999) Constitutive and IFN-gamma regulated expression of IL-7 and IL-15 in human renal cell cancer. Int J Oncol 14: 23-31.
27. Kaplan MH, Grusby MJ (1998) Regulation of T helper cell differentiation by STAT molecules. J Leukoc Biol 61: 2-5.
28. Zhou M, Ouyang W (2003) The function role of GATA-3 in Th1 and Th2 differentiation. Immunol Res 28: 25-37.
29. Schwenger GT, Mordvinov VA, Sanderson CJ (2005) Transcription factor GATA-3 is involved in repression of promoter activity of the human interleukin-4 gene. Biochemistry (Mosc) 70: 1065-1069.
30. Zitvogel L, Terme M, Borg C, Trinchieri G (2006) Dendritic cell-NK cell crosstalk: regulation and physiopathology. Curr Top Microbiol Immunol 298: 157-174.
31. Cavaillon JM (1994) Cytokines and macrophages. Biomed Pharmacother 48: 445-453.
32. Kim DH, Yoo KH, Choi KS, Choi J, Choi SY, et al. (2005) Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 31: 119-126.
33. Barton BE (2006) STAT3: a potential therapeutic target in dendritic cells for the induction of transplant tolerance. Expert Opin Ther Targets 10: 459-470.
34. Brandt K, Bulfone-Paus S, Foster DC, Ruckert R (2003) Interleukin-21 inhibits dendritic cell activation and maturation. Blood 102: 4090-4098.
35. Brady J, Hayakawa Y, Smyth MJ, Nutt SL (2004) IL-21 induces the functional maturation of murine NK cells. J Immunol 172: 2048-2058.
36. Cai G, Kastelein RA, Hunter CA (1999) IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-gamma when combined with IL-18. Eur J Immunol 29: 2658-2665.
37. LeMaoult J, Rouas-Freiss N, Carosella ED (2005) Immuno-tolerogenic functions of HLA-G: relevance in transplantation and oncology, Autoimmun Rev 4: 503-509.
38. Lidstrom C, Matthiesen L, Berg G, Sharma S, Ernerudh J, et al. (2003) Cytokine secretion patterns of NK cells and macrophages in early human pregnancy decidua and blood: implications for suppressor macrophages in decidua. Am J Reprod Immunol 50: 444-452.
39. Vacca P, Pietra G, Falco M, Romeo E, Bottino C, et al. (2006) Analysis of natural killer cells isolated from human decidua: Evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-cell function. Blood 108: 4078-4085.
40. Chaouat G, Zourbas S, Ostojic S, Lappree-Delage G, Dubanchet S, et al. (2002) A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J Reprod Immunol 53: 241-256.
41. Le Bouteiller P, Solier C, Proll J, Aguerre-Girr M, Fournel S, et al. (1999) Placental HLA-G protein expression in vivo: where and what for? Hum Reprod Update 5: 223-233.
42. Burkett PR, Koka R, Chien M, Chai S, Chan F, et al. (2003) IL-15R alpha expression on CD8+ T cells is dispensable for T cell memory. Proc Natl Acad Sci U S A 100: 4724-4729.
43. Kobayashi H, Dubois S, Sato N, Sabzevari H, Sakai Y, et al. (2005) Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance. Blood 105: 721-727.
44. Koka R, Burkett PR, Chien M, Chai S, Chan F, et al. (2003) Interleukin (IL)-15R [alpha]-deficient natural killer cells survive in normal but not IL-15R[alpha]-deficient mice. J Exp Med 197: 977-984.
45. Sivori S, Falco M, Marcenaro E, Parolini S, Biassoni R, et al. (2002) Early expression of triggering receptors and regulatory role of 2B4 in human natural killer cell precursors undergoing in vitro differentiation. Proc Natl Acad Sci U S A 99: 4526-4531.
46. Walzer T, Blery M, Chaix J, Fuseri N, Chasson L, et al. (2007) Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Natl Acad Sci U S A 104: 3384-3389.
47. Yang JS, Xu LY, Huang YM, Van Der Meide PH, Link H, et al. (2000) Adherent dendritic cells expressing high levels of interleukin-10 and low levels of interleukin-12 induce antigen-specific tolerance to experimental autoimmune encephalomyelitis. Immunology 101; 397-403.
48. Gandhi R, Anderson DE, Weiner HL (2007) Cutting Edge: Immature human dendritic cells express latency-associated peptide and inhibit T cell activation in a TGF-beta-dependent manner. J Immunol 178: 4017-4021.
49. Ostroukhova M, Seguin-Devaux C, Oriss TB, Dixon-McCarthy B, Yang L, et al. (2004) Tolerance induced by inhaled antigen involves CD4(+) T cells expressing membrane-bound TGF-beta and FOXP3. J Clin Invest 114: 28-38.
50. Rebmann V, LeMaoult J, Rouas-Freiss N, Carosella ED, Grosse-Wilde H (2007) Quantification and identification of soluble HLA-G isoforms. Tissue Antigens 69 Suppl 1: 143-149.
51. De Maria A, Fogli M, Mazza S, Basso M, Picciotto A, et al. (2007) Increased natural cytotoxicity receptor expression and relevant IL-10 production in NK cells from chronically infected viremic HCV patients. Eur J Immunol 37: 445-455.
52. Parrish-Novak J, Foster DC, Holly RD, Clegg CH (2002) Interleukin-21 and the IL-21 receptor: novel effectors of NK and T cell responses. J Leukoc Biol 72: 856-863.
53. Harada M, Magara-Koyanagi K, Watarai H, Nagata Y, Ishii Y, et al. (2006) IL-21-induced Bepsilon cell apoptosis mediated by natural killer T cells suppresses IgE responses. J Exp Med 203: 2929-2937.
54. Sivori S, Cantoni C, Parolini S, Marcenaro E, Conte R, et al. (2003) IL-21 induces both rapid maturation of human CD34+ cell precursors towards NK cells and acquisition of surface killer Ig-like receptors. Eur J Immunol 33: 3439-3447.
55. Hunt JS (2006) Stranger in a strange land. Immunol Rev 213: 36-47.
56. Loza MJ, Perussia B (2001) Final steps of natural killer cell maturation: a model for type 1-type 2 differentiation? Nat Immunol 2: 917-924.
57. Leichtman AB (2007) Balancing efficacy and toxicity in kidney-transplant immunosuppression. N Engl J Med 357: 2625-2627.
58. Pittenger MF, Martin BJ (2004) Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 95: 9-20.
59. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, et al. (2005) Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105: 4120-4126.
60. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, et al. (2007) Mesenchymal stem cells inhibit natural killer cell proliferation, cytotoxicity and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood.