Cytoskeletal stabilization of inhibitory interactions in immunologic synapses of mature human dendritic cells with natural killer cells

Blood

Volumn 118, Issue 25, 2011, Pages 6487-6498

  Da Silva, Rosa Barreira ^a,b   Graf, Claudine ^c   Münz, Christian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR;

ARTICLE; ASSAY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOSKELETON; CYTOTOXICITY; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; IMMUNOREACTIVITY; INHIBITION KINETICS; NATURAL KILLER CELL; POLARIZATION; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; SIGNAL TRANSDUCTION;

EID: 84055223122     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-07-366328     Document Type: Article

References (48)

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245-252. (Pubitemid 28155090)
2. Alvarez D, Vollmann EH, von Andrian UH. Mechanisms and consequences of dendritic cell migration. Immunity. 2008;29(3):325-342.
3. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Münz C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med. 2002;195(3):343-351. (Pubitemid 34461492)
4. Caux C, Massacrier C, Vanbervliet B, et al. Activation of human dendritic cells through CD40 cross-linking. J Exp Med. 1994;180(4):1263-1272. (Pubitemid 24289600)
5. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med. 1996;184(2):747-752. (Pubitemid 26324129)
6. Reis e Sousa C, Hieny S, Scharton-Kersten T, et al. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J Exp Med. 1997;186(11):1819-1829. (Pubitemid 27524592)
7. Ferlazzo G, Pack M, Thomas D, et al. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci U S A. 2004;101(47):16606-16611. (Pubitemid 39557760)
8. Bajenoff M, Breart B, Huang AY, et al. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J Exp Med. 2006;203(3):619-631.
9. Garrod KR, Wei SH, Parker I, Cahalan MD. Natural killer cells actively patrol peripheral lymph nodes forming stable conjugates to eliminate MHC-mismatched targets. Proc Natl Acad Sci U SA. 2007;104(29):12081-12086. (Pubitemid 47185633)
10. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity. 2007;26(4):503-517. (Pubitemid 46602996)
11. Schleicher U, Liese J, Knippertz I, et al. NK cell activation in visceral leishmaniasis requires TLR9, myeloid DCs, and IL-12, but is independent of plasmacytoid DCs. J Exp Med. 2007;204(4):893-906. (Pubitemid 46631617)
12. Kassim SH, Rajasagi NK, Zhao X, Chervenak R, Jennings SR. In vivo ablation of CD11c-positive dendritic cells increases susceptibility to herpes simplex virus type 1 infection and diminishes NK and T-cell responses. J Virol. 2006;80(8):3985-3993.
13. Mortier E, Woo T, Advincula R, Gozalo S, Ma A. IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med. 2008;205(5):1213-1225. (Pubitemid 351679694)
14. Kang SJ, Liang HE, Reizis B, Locksley RM. Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity. 2008;29(5):819-833.
15. Hou B, Reizis B, DeFranco AL. Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and -extrinsic mechanisms. Immunity. 2008;29(2):272-282.
16. Strowig T, Brilot F, Arrey F, et al. Tonsilar NK cells restrict B cell transformation by the Epstein-Barr virus via IFN-gamma. PLoS Pathog. 2008;4(2):e27.
17. Gerosa F, Gobbi A, Zorzi P, et al. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J Immunol. 2005;174(2):727-734. (Pubitemid 40094266)
18. Andoniou CE, van Dommelen SL, Voigt V, et al. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat Immunol. 2005;6(10):1011-1019. (Pubitemid 41486186)
19. Fernandez NC, Lozier A, Flament C, et al. Dendritic cells directly trigger NK cell functions: crosstalk relevant in innate anti-tumor immune responses in vivo. Nat Med. 1999;5(4):405-411. (Pubitemid 29180578)
20. Nguyen KB, Salazar-Mather TP, Dalod MY, et al. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol. 2002;169(8):4279-4287. (Pubitemid 35178200)
21. Brilot F, Strowig T, Roberts SM, Arrey F, Münz C. NK cell survival mediated through the regulatory synapse with human DCs requires IL-15Ralpha. J Clin Invest. 2007;117(11):3316-3329. (Pubitemid 350096988)
22. Huntington ND, Legrand N, Alves NL, et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med. 2009;206(1):25-34.
23. Medema JP, Schuurhuis DH, Rea D, et al. Expression of the serpin serine protease inhibitor 6 protects dendritic cells from cytotoxic T lymphocyte-induced apoptosis: differential modulation by T helper type 1 and type 2 cells. J Exp Med. 2001;194(5):657-667. (Pubitemid 32844775)
24. Orange JS, Harris KE, Andzelm MM, Valter MM, Geha RS, Strominger JL. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci U S A. 2003;100(24):14151-14156. (Pubitemid 37499206)
25. Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol. 2008;8(9):713-725.
26. Carpen O, Virtanen I, Lehto VP, Saksela E. Polarization of NK cell cytoskeleton upon conjugation with sensitive target cells. J Immunol. 1983;131(6):2695-2698. (Pubitemid 14208816)
27. Vyas YM, Maniar H, Dupont B. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol Rev. 2002;189:161-178. (Pubitemid 35448951)
28. Benninger RK, Vanherberghen B, Young S, et al. Live cell linear dichroism imaging reveals extensive membrane ruffling within the docking structure of natural killer cell immune synapses. Biophys J. 2009;96(2):L13-15.
29. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM. Centrosome polarization delivers secretory granules to the immunological synapse. Nature. 2006;443(7110):462-465. (Pubitemid 44477283)
30. Geiger B, Rosen D, Berke G. Spatial relationships of microtubule- organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J Cell Biol. 1982;95(1):137-143. (Pubitemid 13197083)
31. Borg C, Jalil A, Laderach D, et al. NK cell activation by dendritic cells (DCs) requires the formation of a synapse leading to IL-12 polarization in DCs. Blood. 2004;104(10):3267-3275. (Pubitemid 39507145)
32. Long EO. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol Rev. 2008;224:70-84.
33. Thrasher AJ, Burns SO. WASP: a key immunological multitasker. Nat Rev Immunol. 2010;10(3):182-192.
34. Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol. 1987;105(4):1473-1478.
35. Heath WR, Carbone FR. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol. 2009;10(12):1237-1244.
36. Ferlazzo G, Münz C. Dendritic cell interactions with NK cells from different tissues. J Clin Immunol. 2009;29(3):265-273.
37. Giri JG, Ahdieh M, Eisenman J, et al. Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15. EMBO J. 1994;13(12):2822-2830. (Pubitemid 24191692)
38. Bernard J, Harb C, Mortier E, et al. Identification of an interleukin-15alpha receptor-binding site on human interleukin-15. J Biol Chem. 2004;279(23):24313-24322. (Pubitemid 38725294)
39. Stewart CA, Laugier-Anfossi F, Vely F, et al. Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc Natl Acad Sci U S A. 2005;102(37):13224-13229. (Pubitemid 41325005)
40. Maenaka K, Juji T, Nakayama T, et al. Killer cell immunoglobulin receptors and T cell receptors bind peptide-major histocompatibility complex class I with distinct thermodynamic and kinetic properties. J Biol Chem. 1999;274(40):28329-28334.
41. Vamosi G, Bodnar A, Vereb G, et al. IL-2 and IL-15 receptor alpha-subunits are coexpressed in a supramolecular receptor cluster in lipid rafts of T cells. Proc Natl Acad Sci U S A. 2004;101(30):11082-11087. (Pubitemid 38989587)
42. Morone N, Fujiwara T, Murase K, et al. Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J Cell Biol. 2006;174(6):851-862. (Pubitemid 44373734)
43. Umemura YM, Vrljic M, Nishimura SY, Fujiwara TK, Suzuki KG, Kusumi A. Both MHC class II and its GPI-anchored form undergo hop diffusion as observed by single-molecule tracking. Biophys J. 2008;95(1):435-450.
44. Standeven LJ, Carlin LM, Borszcz P, Davis DM, Burshtyn DN. The actin cytoskeleton controls the efficiency of killer Ig-like receptor accumulation at inhibitory NK cell immune synapses. J Immunol. 2004;173(9):5617-5625. (Pubitemid 39392149)
45. Orange JS, Ramesh N, Remold-O'Donnell E, et al. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc Natl Acad Sci U S A. 2002;99(17):11351-11356. (Pubitemid 34920929)
46. Billadeau DD, Nolz JC, Gomez TS. Regulation of T-cell activation by the cytoskeleton. Nat Rev Immunol. 2007;7(2):131-143. (Pubitemid 46174860)
47. Al-Alwan MM, Rowden G, Lee TD, West KA. The dendritic cell cytoskeleton is critical for the formation of the immunological synapse. J Immunol. 2001;166(3):1452-1456. (Pubitemid 32114622)
48. Turley SJ, Inaba K, Garrett WS, et al. Transport of peptide-MHC class II complexes in developing dendritic cells. Science. 2000;288(5465):522-527. (Pubitemid 30236035)