Priming of Natural Killer Cells by Nonmucosal Mononuclear Phagocytes Requires Instructive Signals from Commensal Microbiota

Immunity

Volumn 37, Issue 1, 2012, Pages 171-186

  Ganal, Stephanie C ^a   Sanos, Stephanie L ^a,e   Kallfass, Carsten ^a   Oberle, Karin ^a   Johner, Caroline ^b   Kirschning, Carsten ^c   Lienenklaus, Stefan ^d   Weiss, Siegfried ^d   Staeheli, Peter ^a   Aichele, Peter ^a   Diefenbach, Andreas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^e Bavarian Nordic GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS INFECTION; GENE EXPRESSION REGULATION; IMMUNOSTIMULATION; INTRACELLULAR SIGNALING; LYMPHOID ORGAN; MICROFLORA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; SIGNAL TRANSDUCTION; VIRUS IMMUNITY;

ANIMALS; CYTOKINES; INTERFERON TYPE I; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; METAGENOME; MICE; MICE, INBRED C57BL; PHAGOCYTES; VIRUS DISEASES;

EID: 84864322646     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.05.020     Document Type: Article

References (61)

1. Arase H., Mocarski E.S., Campbell A.E., Hill A.B., Lanier L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002, 296:1323-1326.
2. Arneson L.N., Segovis C.M., Gomez T.S., Schoon R.A., Dick C.J., Lou Z., Billadeau D.D., Leibson P.J. Dynamin 2 regulates granule exocytosis during NK cell-mediated cytotoxicity. J. Immunol. 2008, 181:6995-7001.
3. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 2008, 8:411-420.
4. Bach J.F. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 2002, 347:911-920.
5. Bauer H., Horowitz R.E., Levenson S.M., Popper H. The response of the lymphatic tissue to the microbial flora. Studies on germfree mice. Am. J. Pathol. 1963, 42:471-483.
6. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., Salazar-Mather T.P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 1999, 17:189-220.
7. Brown M.G., Dokun A.O., Heusel J.W., Smith H.R., Beckman D.L., Blattenberger E.A., Dubbelde C.E., Stone L.R., Scalzo A.A., Yokoyama W.M. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001, 292:934-937.
8. Chen J., Ivashkiv L.B. IFN-γ abrogates endotoxin tolerance by facilitating Toll-like receptor-induced chromatin remodeling. Proc. Natl. Acad. Sci. USA 2010, 107:19438-19443.
9. Clarke T.B., Davis K.M., Lysenko E.S., Zhou A.Y., Yu Y., Weiser J.N. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 2010, 16:228-231.
10. Conrad M.L., Ferstl R., Teich R., Brand S., Blümer N., Yildirim A.O., Patrascan C.C., Hanuszkiewicz A., Akira S., Wagner H., et al. Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J. Exp. Med. 2009, 206:2869-2877.
11. De Somer P., Billiau A. Interferon production by the spleen of rats after intravenous injection of Sindbis virus or heat-killed Escherichia coli. Arch. Gesamte Virusforsch. 1966, 19:143-154.
12. Degli-Esposti M.A., Smyth M.J. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 2005, 5:112-124.
13. Fehniger T.A., Cai S.F., Cao X., Bredemeyer A.J., Presti R.M., French A.R., Ley T.J. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007, 26:798-811.
14. Fernandez N.C., Treiner E., Vance R.E., Jamieson A.M., Lemieux S., Raulet D.H. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 2005, 105:4416-4423.
15. Foster S.L., Hargreaves D.C., Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 2007, 447:972-978.
16. Hargreaves D.C., Horng T., Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009, 138:129-145.
17. Hayakawa Y., Smyth M.J. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 2006, 176:1517-1524.
18. Herberman R.B., Nunn M.E., Lavrin D.H. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int. J. Cancer 1975, 16:216-229.
19. Hill D.A., Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Annu. Rev. Immunol. 2010, 28:623-667.
20. Hooper L.V., Macpherson A.J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 2010, 10:159-169.
21. Huh N.D., Kim Y.B., Koren H.S., Amos D.B. Natural killing and antibody-dependent cellular cytotoxicity in specific-pathogen-free miniature swine and germ-free piglets. II. Ontogenic development development of NK and ADCC. Int. J. Cancer 1981, 28:175-178.
22. Huntington N.D., Tabarias H., Fairfax K., Brady J., Hayakawa Y., Degli-Esposti M.A., Smyth M.J., Tarlinton D.M., Nutt S.L. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J. Immunol. 2007, 178:4764-4770.
23. Ichinohe T., Pang I.K., Kumamoto Y., Peaper D.R., Ho J.H., Murray T.S., Iwasaki A. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 2011, 108:5354-5359.
24. Ito Y., Nisiyama Y., Shimokata K., Kimura Y., Nagata I. Interferon-producing capacity of germfree mice. Infect. Immun. 1976, 13:332-336.
25. Janeway C.A. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 1989, 54:1-13.
26. Kang S.J., Liang H.E., Reizis B., Locksley R.M. Regulation of hierarchical clustering and activation of innate immune cells by dendritic cells. Immunity 2008, 29:819-833.
27. Kawai T., Akira S. Innate immune recognition of viral infection. Nat. Immunol. 2006, 7:131-137.
28. Kim S., Poursine-Laurent J., Truscott S.M., Lybarger L., Song Y.J., Yang L., French A.R., Sunwoo J.B., Lemieux S., Hansen T.H., Yokoyama W.M. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005, 436:709-713.
29. Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011, 334:1561-1565.
30. Klose R.J., Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 2006, 31:89-97.
31. Kruys V., Thompson P., Beutler B. Extinction of the tumor necrosis factor locus, and of genes encoding the lipopolysaccharide signaling pathway. J. Exp. Med. 1993, 177:1383-1390.
32. Lienenklaus S., Cornitescu M., Zietara N., Łyszkiewicz M., Gekara N., Jabłónska J., Edenhofer F., Rajewsky K., Bruder D., Hafner M., et al. Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J. Immunol. 2009, 183:3229-3236.
33. Liu K., Waskow C., Liu X., Yao K., Hoh J., Nussenzweig M. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat. Immunol. 2007, 8:578-583.
34. Longhi M.P., Trumpfheller C., Idoyaga J., Caskey M., Matos I., Kluger C., Salazar A.M., Colonna M., Steinman R.M. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J. Exp. Med. 2009, 206:1589-1602.
35. Lucas M., Schachterle W., Oberle K., Aichele P., Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 2007, 26:503-517.
36. Macpherson A.J., Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004, 303:1662-1665.
37. Mattei F., Schiavoni G., Belardelli F., Tough D.F. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J. Immunol. 2001, 167:1179-1187.
38. Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122:107-118.
39. McCartney S., Vermi W., Gilfillan S., Cella M., Murphy T.L., Schreiber R.D., Murphy K.M., Colonna M. Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J. Exp. Med. 2009, 206:2967-2976.
40. Mitsuyama M., Ohara R., Amako K., Nomoto K., Yokokura T., Nomoto K. Ontogeny of macrophage function to release superoxide anion in conventional and germfree mice. Infect. Immun. 1986, 52:236-239.
41. Mørland B., Smievoll A.I., Midtvedt T. Comparison of peritoneal macrophages from germfree and conventional mice. Infect. Immun. 1979, 26:1129-1136.
42. 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, 205:1213-1225.
43. Noverr M.C., Huffnagle G.B. Does the microbiota regulate immune responses outside the gut?. Trends Microbiol. 2004, 12:562-568.
44. Ovchinnikov D.A. Macrophages in the embryo and beyond: much more than just giant phagocytes. Genesis 2008, 46:447-462.
45. Ramirez-Carrozzi V.R., Braas D., Bhatt D.M., Cheng C.S., Hong C., Doty K.R., Black J.C., Hoffmann A., Carey M., Smale S.T. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 2009, 138:114-128.
46. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9:313-323.
47. Saccani S., Pantano S., Natoli G. p38-Dependent marking of inflammatory genes for increased NF-κ B recruitment. Nat. Immunol. 2002, 3:69-75.
48. Sanos S.L., Bui V.L., Mortha A., Oberle K., Heners C., Johner C., Diefenbach A. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 2009, 10:83-91.
49. Santos-Rosa H., Schneider R., Bannister A.J., Sherriff J., Bernstein B.E., Emre N.C., Schreiber S.L., Mellor J., Kouzarides T. Active genes are tri-methylated at K4 of histone H3. Nature 2002, 419:407-411.
50. Scalzo A.A., Fitzgerald N.A., Wallace C.R., Gibbons A.E., Smart Y.C., Burton R.C., Shellam G.R. The effect of the Cmv-1 resistance gene, which is linked to the natural killer cell gene complex, is mediated by natural killer cells. J. Immunol. 1992, 149:581-589.
51. Scheu S., Dresing P., Locksley R.M. Visualization of IFNbeta production by plasmacytoid versus conventional dendritic cells under specific stimulation conditions in vivo. Proc. Natl. Acad. Sci. USA 2008, 105:20416-20421.
52. Shelton E., Daves S., Hemmer R. Quantitation of strain BALB-c mouse peritoneal cells. Science 1970, 168:1232-1234.
53. Smale S.T. Selective transcription in response to an inflammatory stimulus. Cell 2010, 140:833-844.
54. Solodova E., Jablonska J., Weiss S., Lienenklaus S. Production of IFN-β during Listeria monocytogenes infection is restricted to monocyte/macrophage lineage. PLoS ONE 2011, 6:e18543.
55. Tamura T., Yanai H., Savitsky D., Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 2008, 26:535-584.
56. +) innate lymphocytes. Immunity 2010, 33:736-751.
57. Walton K.L., He J., Kelsall B.L., Sartor R.B., Fisher N.C. Dendritic cells in germ-free and specific pathogen-free mice have similar phenotypes and in vitro antigen presenting function. Immunol. Lett. 2006, 102:16-24.
58. Wei G., Wei L., Zhu J., Zang C., Hu-Li J., Yao Z., Cui K., Kanno Y., Roh T.Y., Watford W.T., et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009, 30:155-167.
59. Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., Hu C., Wong F.S., Szot G.L., Bluestone J.A., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008, 455:1109-1113.
60. Wilson N.S., Young L.J., Kupresanin F., Naik S.H., Vremec D., Heath W.R., Akira S., Shortman K., Boyle J., Maraskovsky E., et al. Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol. Cell Biol. 2008, 86:200-205.
61. Wu H.J., Ivanov I.I., Darce J., Hattori K., Shima T., Umesaki Y., Littman D.R., Benoist C., Mathis D. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010, 32:815-827.