Cellular Innate Immunity: An Old Game with New Players

Journal of Innate Immunity

Volumn 9, Issue 2, 2017, Pages 111-125

  Gasteiger, Georg ^a   D'osualdo, Andrea ^e   Schubert, David A ^e   Weber, Alexander ^b   Bruscia, Emanuela M ^d   Hartl, Dominik ^c,e  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Institute for Cell Biology   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Host defense; Immune response; Innate Immunity; Innate lymphoid cells; Macrophages; Myeloid derived suppressor cells; Neutrophils; Pattern recognition receptors; Phagocytosis; Toll like receptor

Indexed keywords

INFLAMMASOME; DNA; PATTERN RECOGNITION RECEPTOR;

ACTIVE IMMUNIZATION; ADAPTIVE IMMUNITY; AUTOIMMUNE DISEASE; AUTOINFLAMMATORY DISEASE; CELLS BY BODY ANATOMY; CELLULAR IMMUNITY; DISEASE TRANSMISSION; GENETIC PROCEDURES; HUMAN; IMMUNOCOMPETENT CELL; INFECTION; INNATE IMMUNITY; LYMPHOID CELL; MACROPHAGE; MOLECULAR PATHOLOGY; MYELOID-DERIVED SUPPRESSOR CELL; NEUTROPHIL; NONHUMAN; REVIEW; ANIMAL; AUTOIMMUNE DISEASES; IMMUNOLOGY; LYMPHOCYTE; METABOLISM; MICROFLORA;

ADAPTIVE IMMUNITY; ANIMALS; AUTOIMMUNE DISEASES; DNA; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; INFECTION; INFLAMMASOMES; LYMPHOCYTES; MICROBIOTA; RECEPTORS, PATTERN RECOGNITION;

EID: 85008392821     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000453397     Document Type: Review

References (231)

1. Buchmann K: Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 2014; 5: 459.
2. Bryant CE, Monie TP: Mice, men and the relatives: cross-species studies underpin innate immunity. Open Biol 2012; 2: 120015.
3. Galli SJ, Borregaard N, Wynn TA: Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol 2011; 12: 1035-1044.
4. Hilchie AL, Wuerth K, Hancock RE: Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nat Chem Biol 2013; 9: 761-768.
5. Bevins CL, Salzman NH: Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 2011; 9: 356-368.
6. Lai Y, Gallo RL: Amped up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 2009; 30: 131-141.
7. Degn SE, Thiel S: Humoral pattern recognition and the complement system. Scand J Immunol 2013; 78: 181-193.
8. de Cordoba SR, Tortajada A, Harris CL, Morgan BP: Complement dysregulation and disease: from genes and proteins to diagnostics and drugs. Immunobiology 2012; 217: 1034-1046.
9. Carroll MC, Isenman DE: Regulation of humoral immunity by complement. Immunity 2012; 37: 199-207.
10. Chan JK, Roth J, Oppenheim JJ, Tracey KJ, Vogl T, Feldmann M, Horwood N, Nanchahal J: Alarmins: awaiting a clinical response. J Clin Invest 2012; 122: 2711-2719.
11. Yang D, de la Rosa G, Tewary P, Oppenheim JJ: Alarmins link neutrophils and dendritic cells. Trends Immunol 2009; 30: 531-537.
12. Sokol CL, Luster AD: The chemokine system in innate immunity. Cold Spring Harb Perspect Biol 2015; 7:a016303.
13. Lee CG, Da Silva CA, Lee JY, Hartl D, Elias JA: Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol 2008; 20: 684-689.
14. van der Meer JW, Joosten LA, Riksen N, Netea MG: Trained immunity: a smart way to enhance innate immune defence. Mol Immunol 2015; 68: 40-44.
15. Martinez-Gonzalez I, Matha L, Steer CA, Ghaedi M, Poon GF, Takei F: Allergen-experienced group 2 innate lymphoid cells acquire memorylike properties and enhance allergic lung inflammation. Immunity 2016; 45: 198-208.
16. O'Leary JG, Goodarzi M, Drayton DL, von Andrian UH: T cell-and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 2006; 7: 507-516.
17. Sun JC, Beilke JN, Lanier LL: Adaptive immune features of natural killer cells. Nature 2009; 457: 557-561.
18. Bedoui S, Gebhardt T, Gasteiger G, Kastenmuller W: Parallels and differences between innate and adaptive lymphocytes. Nat Immunol 2016; 17: 490-494.
19. Burian M, Schittek B: The secrets of dermcidin action. Int J Med Microbiol 2015; 305: 283-286.
20. Schittek B: The multiple facets of dermcidin in cell survival and host defense. J Innate Immun 2012; 4: 349-360.
21. Kawai T, Akira S: The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol 2010; 11: 373-384.
22. Kawai T, Akira S: Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011; 34: 637-650.
23. Pluddemann A, Mukhopadhyay S, Gordon S: Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol Rev 2011; 240: 11-24.
24. Mukhopadhyay S, Gordon S: The role of scavenger receptors in pathogen recognition and innate immunity. Immunobiology 2004; 209: 39-49.
25. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S: Macrophage receptors and immune recognition. Annu Rev Immunol 2005; 23: 901-944.
26. Hornung V, Hartmann R, Ablasser A, Hopfner KP: OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat Rev Immunol 2014; 14: 521-528.
27. Hornung V, Latz E: Intracellular DNA recognition. Nat Rev Immunol 2010; 10: 123-130.
28. Griffith JW, Sokol CL, Luster AD: Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol 2014; 32: 659-702.
29. Gerard C, Rollins BJ: Chemokines and disease. Nat Immunol 2001; 2: 108-115.
30. Kruger P, Saffarzadeh M, Weber AN, Rieber N, Radsak M, von Bernuth H, Benarafa C, Roos D, Skokowa J, Hartl D: Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog 2015; 11: e1004651.
31. Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JA, Tesselaar K, Koenderman L: In vivo labeling with 2H 2 O reveals a human neutrophil lifespan of 5.4 days. Blood 2010; 116: 625-627.
32. Brinkmann V, Zychlinsky A: Beneficial suicide: why neutrophils die to make nets. Nat Rev Microbiol 2007; 5: 577-582.
33. Gabrilovich DI, Nagaraj S: Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9: 162-174.
34. Lammermann T: In the eye of the neutrophil swarm-navigation signals that bring neutrophils together in inflamed and infected tissues. J Leukoc Biol 2016; 100: 55-63.
35. Lammermann T, Afonso PV, Angermann BR, Wang JM, Kastenmuller W, Parent CA, Germain RN: Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 2013; 498: 371-375.
36. Zhang D, Chen G, Manwani D, Mortha A, Xu C, Faith JJ, Burk RD, Kunisaki Y, Jang JE, Scheiermann C, Merad M, Frenette PS: Neutrophil ageing is regulated by the microbiome. Nature 2015; 525: 528-532.
37. Hager M, Cowland JB, Borregaard N: Neutrophil granules in health and disease. J Intern Med 2010; 268: 25-34.
38. Yipp BG, Kubes P: NETosis: how vital is it Blood 2013; 122: 2784-2794.
39. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A: Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535.
40. Zychlinsky A: Neutrophil extracellular traps. Eur J Clin Invest 2009; 39: 27-27.
41. Lightfoot YL, Kaplan MJ: Disentangling the role of neutrophil extracellular traps in rheumatic diseases. Curr Opin Rheumatol 2016, E-pub ahead of print.
42. Grayson PC, Kaplan MJ: At the bench: neutrophil extracellular traps (NETs) highlight novel aspects of innate immune system involvement in autoimmune diseases. J Leukoc Biol 2016; 99: 253-264.
43. Barnado A, Crofford LJ, Oates JC: At the bedside: neutrophil extracellular traps (NETs) as targets for biomarkers and therapies in autoimmune diseases. J Leukoc Biol 2016; 99: 265-278.
44. Sorensen OE, Borregaard N: Neutrophil extracellular traps-the dark side of neutrophils. J Clin Invest 2016; 126: 1612-1620.
45. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU: Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 2009; 16: 1438-1444.
46. Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, Robbins SM, Green FH, Surette MG, Sugai M, Bowden MG, Hussain M, Zhang K, Kubes P: A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus . J Immunol 2010; 185: 7413-7425.
47. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, de Boisfleury Chevance A, Zhang K, Conly J, Kubes P: Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012; 18: 1386-1393.
48. Kolaczkowska E, Kubes P: Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013; 13: 159-175.
49. Branzk N, Lubojemska A, Hardison SE, Wang Q, Gutierrez MG, Brown GD, Papayannopoulos V: Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 2014; 15: 1017-1025.
50. Ermert D, Urban CF, Laube B, Goosmann C, Zychlinsky A, Brinkmann V: Mouse neutrophil extracellular traps in microbial infections. J Innate Immun 2009; 1: 181-193.
51. Peschel A, Hartl D: Anuclear neutrophils keep hunting. Nat Med 2012; 18: 1336-1338.
52. Okabe Y, Medzhitov R: Tissue biology perspective on macrophages. Nat Immunol 2016; 17: 9-17.
53. Byrne AJ, Mathie SA, Gregory LG, Lloyd CM: Pulmonary macrophages: key players in the innate defence of the airways. Thorax 2015; 70: 1189-1196.
54. Murray PJ, Wynn TA: Obstacles and opportunities for understanding macrophage polarization. J Leukoc Biol 2011; 89: 557-563.
55. Murray PJ, Wynn TA: Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011; 11: 723-737.
56. Rothlin CV, Carrera-Silva EA, Bosurgi L, Ghosh S: Tam receptor signaling in immune homeostasis. Annu Rev Immunol 2015; 33: 355-391.
57. Anwar MA, Basith S, Choi S: Negative regulatory approaches to the attenuation of toll-like receptor signaling. Exp Mol Med 2013; 45:e11.
58. Bourdonnay E, Zaslona Z, Penke LR, Speth JM, Schneider DJ, Przybranowski S, Swanson JA, Mancuso P, Freeman CM, Curtis JL, Peters-Golden M: Transcellular delivery of vesicular SOCS proteins from macrophages to epithelial cells blunts inflammatory signaling. J Exp Med 2015; 212: 729-742.
59. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, MacDonald AS, Allen JE: Local macrophage proliferation, rather than recruitment from the blood, is a signature of Th2 inflammation. Science 2011; 332: 1284-1288.
60. Soroosh P, Doherty TA, Duan W, Mehta AK, Choi H, Adams YF, Mikulski Z, Khorram N, Rosenthal P, Broide DH, Croft M: Lung-resident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J Exp Med 2013; 210: 775-788.
61. Westphalen K, Gusarova GA, Islam MN, Subramanian M, Cohen TS, Prince AS, Bhattacharya J: Sessile alveolar macrophages communicate with alveolar epithelium to modulate immunity. Nature 2014; 506: 503-506.
62. Hussell T, Bell TJ: Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 2014; 14: 81-93.
63. Lee GR, Bithell TC, Foerster J, Athens JW, Lukens JN (eds): Wintrobe's Clinical Hematology, ed 9. Philadelphia, Lea & Febiger, 1993.
64. van de Laar L, Saelens W, De Prijck S, Martens L, Scott CL, Van Isterdael G, Hoffmann E, Beyaert R, Saeys Y, Lambrecht BN, Guilliams M: Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 2016; 44: 755-768.
65. Perdiguero EG, Geissmann F: The development and maintenance of resident macrophages. Nat Immunol 2016; 17: 2-8.
66. Ginhoux F, Guilliams M: Tissue-resident macrophage ontogeny and homeostasis. Immunity 2016; 44: 439-449.
67. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I: Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 2014; 159: 1312-1326.
68. Auffray C, Fogg DK, Narni-Mancinelli E, Senechal B, Trouillet C, Saederup N, Leemput J, Bigot K, Campisi L, Abitbol M, Molina T, Charo I, Hume DA, Cumano A, Lauvau G, Geissmann F: CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med 2009; 206: 595-606.
69. Wang J, Kubes P: A reservoir of mature cavity macrophages that can rapidly invade visceral organs to affect tissue repair. Cell 2016; 165: 668-678.
70. Wynn TA, Vannella KM: Macrophages in tissue repair, regeneration, and fibrosis. Immunity 2016; 44: 450-462.
71. Sica A, Mantovani A: Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122: 787-795.
72. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M: Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013; 229: 176-185.
73. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, De Nardo D, Gohel TD, Emde M, Schmidleithner L, Ganesan H, Nino-Castro A, Mallmann MR, Labzin L, Theis H, Kraut M, Beyer M, Latz E, Freeman TC, Ulas T, Schultze JL: Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 2014; 40: 274-288.
74. Turner M, Galloway A, Vigorito E: Noncoding RNA and its associated proteins as regulatory elements of the immune system. Nat Immunol 2014; 15: 484-491.
75. Glass CK, Natoli G: Molecular control of activation and priming in macrophages. Nat Immunol 2016; 17: 26-33.
76. Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O'Neill LA, Xavier RJ: Trained immunity: a program of innate immune memory in health and disease. Science 2016; 352:aaf1098.
77. Greten TF, Manns MP, Korangy F: Myeloid derived suppressor cells in human diseases. Int Immunopharmacol 2011; 11: 802-807.
78. Mantovani A: The growing diversity and spectrum of action of myeloid-derived suppressor cells. Eur J Immunol 2010; 40: 3317-3320.
79. Brandau S, Moses K, Lang S: The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: cousins, siblings or twins Semin Cancer Biol 2013; 23: 171-182.
80. Dumitru CA, Moses K, Trellakis S, Lang S, Brandau S: Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology. Cancer Immunol Immunother 2012; 61: 1155-1167.
81. Bronte V, Brandau S, Chen SH, Colombo MP, Frey AB, Greten TF, Mandruzzato S, Murray PJ, Ochoa A, Ostrand-Rosenberg S, Rodriguez PC, Sica A, Umansky V, Vonderheide RH, Gabrilovich DI: Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun 2016; 7: 12150.
82. Nagaraj S, Gabrilovich DI: Myeloid-derived suppressor cells. Adv Exp Med Biol 2007; 601: 213-223.
83. Youn JI, Gabrilovich DI: The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 2010; 40: 2969-2975.
84. Gantt S, Gervassi A, Jaspan H, Horton H: The role of myeloid-derived suppressor cells in immune ontogeny. Front Immunol 2014; 5: 387.
85. Ost M, Singh A, Peschel A, Mehling R, Rieber N, Hartl D: Myeloid-derived suppressor cells in bacterial infections. Front Cell Infect Microbiol 2016; 6: 37.
86. Diefenbach A, Colonna M, Koyasu S: Development, differentiation, and diversity of innate lymphoid cells. Immunity 2014; 41: 354-365.
87. Rankin LC, Girard-Madoux MJ, Seillet C, Mielke LA, Kerdiles Y, Fenis A, Wieduwild E, Putoczki T, Mondot S, Lantz O, Demon D, Papenfuss AT, Smyth GK, Lamkanfi M, Carotta S, Renauld JC, Shi W, Carpentier S, Soos T, Arendt C, Ugolini S, Huntington ND, Belz GT, Vivier E: Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat Immunol 2016; 17: 179-186.
88. Wensveen FM, Jelencic V, Valentic S, Sestan M, Wensveen TT, Theurich S, Glasner A, Mendrila D, Stimac D, Wunderlich FT, Bruning JC, Mandelboim O, Polic B: Nk cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat Immunol 2015; 16: 376-385.
89. Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CGK, Doering TA, Angelosanto JM, Laidlaw BJ, Yang CY, Sathaliyawala T, Kubota M, Turner D, Diamond JM, Goldrath AW, Farber DL, Collman RG, Wherry EJ, Artis D: Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 2011; 12: 1045-1054.
90. Lindemans CA, Calafiore M, Mertelsmann AM, O'Connor MH, Dudakov JA, Jenq RR, Velardi E, Young LF, Smith OM, Lawrence G, Ivanov JA, Fu YY, Takashima S, Hua G, Martin ML, O'Rourke KP, Lo YH, Mokry M, Romera-Hernandez M, Cupedo T, Dow LE, Nieuwenhuis EE, Shroyer NF, Liu C, Kolesnick R, van den Brink MR, Hanash AM: Interleukin-
91. promotes intestinal-stem-cellmediated epithelial regeneration. Nature 2015; 528: 560-564.
92. von Moltke J, Ji M, Liang HE, Locksley RM: Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature 2016; 529: 221-225.
93. Lee MW, Odegaard JI, Mukundan L, Qiu Y, Molofsky AB, Nussbaum JC, Yun K, Locksley RM, Chawla A: Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 2015; 160: 74-87.
94. Molofsky AB, Nussbaum JC, Liang HE, Van Dyken SJ, Cheng LE, Mohapatra A, Chawla A, Locksley RM: Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med 2013; 210: 535-549.
95. Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M: Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014; 343: 1249288.
96. Gasteiger G, Fan X, Dikiy S, Lee SY, Rudensky AY: Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 2015; 350: 981-985.
97. Moro K, Kabata H, Tanabe M, Koga S, Takeno N, Mochizuki M, Fukunaga K, Asano K, Betsuyaku T, Koyasu S: Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat Immunol 2016; 17: 76-86.
98. Klose CS, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, Fabiunke C, Pfeifer D, Sexl V, Fonseca-Pereira D, Domingues RG, Veiga-Fernandes H, Arnold SJ, Busslinger M, Dunay IR, Tanriver Y, Diefenbach A: Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014; 157: 340-356.
99. Constantinides MG, McDonald BD, Verhoef PA, Bendelac A: A committed precursor to innate lymphoid cells. Nature 2014; 508: 397-401.
100. Shih HY, Sciume G, Mikami Y, Guo L, Sun HW, Brooks SR, Urban JF Jr, Davis FP, Kanno Y, O'Shea JJ: Developmental acquisition of regulomes underlies innate lymphoid cell functionality. Cell 2016; 165: 120-133.
101. Gronke K, Kofoed-Nielsen M, Diefenbach A: Innate lymphoid cells, precursors and plasticity. Immunol Lett 2016; 179: 9-18.
102. Gasteiger G, Rudensky AY: Interactions between innate and adaptive lymphocytes. Nat Rev Immunol 2014; 14: 631-639.
103. Hepworth MR, Sonnenberg GF: Regulation of the adaptive immune system by innate lymphoid cells. Curr Opin Immunol 2014; 27: 75-82.
104. Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH, Brewer JM, Englezakis A, Barlow JL, Hams E, Scanlon ST, Ogg GS, Fallon PG, McKenzie AN: MHCII-mediated dialogue between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 2014; 41: 283-295.
105. Gasteiger G, Hemmers S, Bos PD, Sun JC, Rudensky AY: IL-2-dependent adaptive control of NK cell homeostasis. J Exp Med 2013; 210: 1179-1187.
106. Halim TY, Hwang YY, Scanlon ST, Zaghouani H, Garbi N, Fallon PG, McKenzie AN: Group 2 innate lymphoid cells license dendritic cells to potentiate memory Th2 cell responses. Nat Immunol 2016; 17: 57-64.
107. Halim TY, Steer CA, Matha L, Gold MJ, Martinez-Gonzalez I, McNagny KM, Mc-Kenzie AN, Takei F: Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 2014; 40: 425-435.
108. Withers DR, Gaspal FM, Mackley EC, Marriott CL, Ross EA, Desanti GE, Roberts NA, White AJ, Flores-Langarica A, McConnell FM, Anderson G, Lane PJ: Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J Immunol 2012; 189: 2094-2098.
109. Hepworth MR, Fung TC, Masur SH, Kelsen JR, McConnell FM, Dubrot J, Withers DR, Hugues S, Farrar MA, Reith W, Eberl G, Baldassano RN, Laufer TM, Elson CO, Sonnenberg GF: Immune tolerance. Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4(+) T cells. Science 2015; 348: 1031-1035.
110. Mackley EC, Houston S, Marriott CL, Halford EE, Lucas B, Cerovic V, Filbey KJ, Maizels RM, Hepworth MR, Sonnenberg GF, Milling S, Withers DR: CCR7-dependent trafficking of ROR(+) ILCs creates a unique microenvironment within mucosal draining lymph nodes. Nat Commun 2015; 6: 5862.
111. Serafini N, Vosshenrich CA, Di Santo JP: Transcriptional regulation of innate lymphoid cell fate. Nat Rev Immunol 2015; 15: 415-428.
112. Eberl G, Colonna M, Di Santo JP, McKenzie AN: Innate lymphoid cells: a new paradigm in immunology. Science 2015; 348:aaa6566.
113. McKenzie AN, Spits H, Eberl G: Innate lymphoid cells in inflammation and immunity. Immunity 2014; 41: 366-374.
114. Martinon F, Mayor A, Tschopp J: The inflammasomes: guardians of the body. Annu Rev Immunol 2009; 27: 229-265.
115. Kanneganti TD: The inflammasome: firing up innate immunity. Immunol Rev 2015; 265: 1-5.
116. Rathinam VA, Fitzgerald KA: Inflammasome complexes: emerging mechanisms and effector functions. Cell 2016; 165: 792-800.
117. Lu A, Magupalli VG, Ruan J, Yin Q, Atianand MK, Vos MR, Schroder GF, Fitzgerald KA, Wu H, Egelman EH: Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 2014; 156: 1193-1206.
118. Bergsbaken T, Fink SL, Cookson BT: Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009; 7: 99-109.
119. Man SM, Kanneganti TD: Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat Rev Immunol 2016; 16: 7-21.
120. Shi J, Zhao Y, Wang Y, Gao W, Ding J, Li P, Hu L, Shao F: Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 2014; 514: 187-192.
121. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, Zhang J, Lee WP, Roose-Girma M, Dixit VM: Non-canonical inflammasome activation targets caspase-11. Nature 2011; 479: 117-121.
122. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F: Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015; 526: 660-665.
123. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM: Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 2015; 526: 666-671.
124. Gurung P, Kanneganti TD: Novel roles for caspase-8 in IL-1 and inflammasome regulation. Am J Pathol 2015; 185: 17-25.
125. Jo EK, Kim JK, Shin DM, Sasakawa C: Molecular mechanisms regulating NLRP3 inflammasome activation. Cell Mol Immunol 2016; 13: 148-159.
126. Py BF, Kim MS, Vakifahmetoglu-Norberg H, Yuan J: Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol Cell 2013; 49: 331-338.
127. Spalinger MR, Kasper S, Gottier C, Lang S, Atrott K, Vavricka SR, Scharl S, Gutte PM, Grutter MG, Beer HD, Contassot E, Chan AC, Dai X, Rawlings DJ, Mair F, Becher B, Falk W, Fried M, Rogler G, Scharl M: NLRP3 tyrosine phosphorylation is controlled by protein tyrosine phosphatase PTPN22. J Clin Invest 2016; 126: 1783-1800.
128. Lee GS, Subramanian N, Kim AI, Aksentijevich I, Goldbach-Mansky R, Sacks DB, Germain RN, Kastner DL, Chae JJ: The calcium-sensing receptor regulates the NLRP3 inflammasome through CA2+ and cAMP. Nature 2012; 492: 123-127.
129. Gaidt MM, Ebert TS, Chauhan D, Schmidt T, Schmid-Burgk JL, Rapino F, Robertson AA, Cooper MA, Graf T, Hornung V: Human monocytes engage an alternative inflammasome pathway. Immunity 2016; 44: 833-846.
130. Gaidt MM, Ebert TS, Chauhan D, Schmidt T, Schmid-Burgk JL, Rapino F, Robertson AAB, Cooper MA, Graf T, Hornung V: Human monocytes engage an alternative inflammasome pathway. Immunity 2016; 44: 833-846.
131. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszynski A, Forsberg LS, Carlson RW, Dixit VM: Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 2013; 341: 1246-1249.
132. Ito M, Shichita T, Okada M, Komine R, Noguchi Y, Yoshimura A, Morita R: Bruton's tyrosine kinase is essential for NLRP3 inflammasome activation and contributes to ischaemic brain injury. Nat Commun 2015; 6: 7360.
133. He Y, Zeng MY, Yang D, Motro B, Nunez G: Nek7 is an essential mediator of NLRP3 activation downstream of potassium efflux. Nature 2016; 530: 354-357.
134. Wolf AJ, Reyes CN, Liang W, Becker C, Shimada K, Wheeler ML, Cho HC, Popescu NI, Coggeshall KM, Arditi M, Underhill DM: Hexokinase is an innate immune receptor for the detection of bacterial peptidoglycan. Cell 2016; 166: 624-636.
135. O'Neill LA, Kishton RJ, Rathmell J: A guide to immunometabolism for immunologists. Nat Rev Immunol 2016; 16: 553-565.
136. Ravindran R, Loebbermann J, Nakaya HI, Khan N, Ma H, Gama L, Machiah DK, Lawson B, Hakimpour P, Wang YC, Li S, Sharma P, Kaufman RJ, Martinez J, Pulendran B: The amino acid sensor GCN2 controls gut inflammation by inhibiting inflammasome activation. Nature 2016; 531: 523-527.
137. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, Frezza C, Bernard NJ, Kelly B, Foley NH, Zheng L, Gardet A, Tong Z, Jany SS, Corr SC, Haneklaus M, Caffrey BE, Pierce K, Walmsley S, Beasley FC, Cummins E, Nizet V, Whyte M, Taylor CT, Lin H, Masters SL, Gottlieb E, Kelly VP, Clish C, Auron PE, Xavier RJ, O'Neill LA: Succinate is an inflammatory signal that induces IL-1 through HIF-1. Nature 2013; 496: 238-242.
138. Guo C, Xie S, Chi Z, Zhang J, Liu Y, Zhang L, Zheng M, Zhang X, Xia D, Ke Y, Lu L, Wang D: Bile acids control inflammation and metabolic disorder through inhibition of NLRP3 inflammasome. Immunity 2016; 45: 944.
139. Mills EL, Kelly B, Logan A, Costa AS, Varma M, Bryant CE, Tourlomousis P, Dabritz JH, Gottlieb E, Latorre I, Corr SC, McManus G, Ryan D, Jacobs HT, Szibor M, Xavier RJ, Braun T, Frezza C, Murphy MP, O'Neill LA: Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell 2016; 167: 457-470 e413.
140. Bruchard M, Rebe C, Derangere V, Togbe D, Ryffel B, Boidot R, Humblin E, Hamman A, Chalmin F, Berger H, Chevriaux A, Limagne E, Apetoh L, Vegran F, Ghiringhelli F: The receptor NLRP3 is a transcriptional regulator of Th2 differentiation. Nat Immunol 2015; 16: 859-870.
141. Feldmeyer L, Keller M, Niklaus G, Hohl D, Werner S, Beer HD: The inflammasome mediates UVB-induced activation and secretion of interleukin-1 by keratinocytes. Curr Biol 2007; 17: 1140-1145.
142. Dombrowski Y, Peric M, Koglin S, Kammerbauer C, Goss C, Anz D, Simanski M, Glaser R, Harder J, Hornung V, Gallo RL, Ruzicka T, Besch R, Schauber J: Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci Transl Med 2011; 3: 82ra38.
143. Shaw PJ, Lukens JR, Burns S, Chi H, McGargill MA, Kanneganti TD: Cutting edge: critical role for PYCARD/ASC in the development of experimental autoimmune encephalomyelitis. J Immunol 2010; 184: 4610-4614.
144. Martin BN, Wang C, Zhang CJ, Kang Z, Gulen MF, Zepp JA, Zhao J, Bian G, Do JS, Min B, Pavicic PG Jr, El-Sanadi C, Fox PL, Akitsu A, Iwakura Y, Sarkar A, Wewers MD, Kaiser WJ, Mocarski ES, Rothenberg ME, Hise AG, Dubyak GR, Ransohoff RM, Li X: T cell-intrinsic ASC critically promotes Th17-mediated experimental autoimmune encephalomyelitis. Nat Immunol 2016; 17: 583-592.
145. Kuemmerle-Deschner JB: CAPS-pathogenesis, presentation and treatment of an autoinflammatory disease. Semin Immunopathol 2015; 37: 377-385.
146. Guo H, Callaway JB, Ting JP: Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 2015; 21: 677-687.
147. Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O, Hunt PW, Hatano H, Sowinski S, Munoz-Arias I, Greene WC: Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014; 505: 509-514.
148. Sagoo P, Garcia Z, Breart B, Lemaitre F, Michonneau D, Albert ML, Levy Y, Bousso P: In vivo imaging of inflammasome activation reveals a subcapsular macrophage burst response that mobilizes innate and adaptive immunity. Nat Med 2016; 22: 64-71.
149. Kastenmuller W, Torabi-Parizi P, Subramanian N, Lammermann T, Germain RN: A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 2012; 150: 1235-1248.
150. Coll RC, Robertson AA, Chae JJ, Higgins SC, Munoz-Planillo R, Inserra MC, Vetter I, Dungan LS, Monks BG, Stutz A, Croker DE, Butler MS, Haneklaus M, Sutton CE, Nunez G, Latz E, Kastner DL, Mills KH, Masters SL, Schroder K, Cooper MA, O'Neill LA: A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat Med 2015; 21: 248-255.
151. Kawai T, Akira S: The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol 2010; 11: 373-384.
152. Kato H, Takahasi K, Fujita T: RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 2011; 243: 91-98.
153. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, Lu Y, Miyagishi M, Kodama T, Honda K, Ohba Y, Taniguchi T: DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007; 448: 501-505.
154. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, Bowie AG: IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010; 11: 997-1004.
155. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ: The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 2011; 12: 959-965.
156. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES: AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009; 458: 509-513.
157. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, Latz E, Fitzgerald KA: AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009; 458: 514-518.
158. Sun L, Wu J, Du F, Chen X, Chen ZJ: Cyclic gmp-amp synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339: 786-791.
159. Wu J, Sun L, Chen X, Du F, Shi H, Chen C, Chen ZJ: Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013; 339: 826-830.
160. Civril F, Deimling T, de Oliveira Mann CC, Ablasser A, Moldt M, Witte G, Hornung V, Hopfner KP: Structural mechanism of cytosolic DNA sensing by cGAS. Nature 2013; 498: 332-337.
161. Gao P, Ascano M, Wu Y, Barchet W, Gaffney BL, Zillinger T, Serganov AA, Liu Y, Jones RA, Hartmann G, Tuschl T, Patel DJ: Cyclic [G(2,5 )pA(3 ,5 )p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 2013; 153: 1094-1107.
162. Li X, Shu C, Yi G, Chaton CT, Shelton CL, Diao J, Zuo X, Kao CC, Herr AB, Li P: Cyclic GMP-AMP synthase is activated by doublestranded DNA-induced oligomerization. Immunity 2013; 39: 1019-1031.
163. Ablasser A, Goldeck M, Cavlar T, Deimling T, Witte G, Rohl I, Hopfner KP, Ludwig J, Hornung V: cGAS produces a 2 -5 -linked cyclic dinucleotide second messenger that activates STING. Nature 2013; 498: 380-384.
164. Diner EJ, Burdette DL, Wilson SC, Monroe KM, Kellenberger CA, Hyodo M, Hayakawa Y, Hammond MC, Vance RE: The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep 2013; 3: 1355-1361.
165. Zhang X, Shi H, Wu J, Zhang X, Sun L, Chen C, Chen ZJ: Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 2013; 51: 226-235.
166. Ablasser A, Schmid-Burgk JL, Hemmerling I, Horvath GL, Schmidt T, Latz E, Hornung V: Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature 2013; 503: 530-534.
167. Bridgeman A, Maelfait J, Davenne T, Partridge T, Peng Y, Mayer A, Dong T, Kaever V, Borrow P, Rehwinkel J: Viruses transfer the antiviral second messenger cGAMP between cells. Science 2015; 349: 1228-1232.
168. Gentili M, Kowal J, Tkach M, Satoh T, Lahaye X, Conrad C, Boyron M, Lombard B, Durand S, Kroemer G, Loew D, Dalod M, Thery C, Manel N: Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science 2015; 349: 1232-1236.
169. Ishikawa H, Ma Z, Barber GN: Sting regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461: 788-792.
170. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV, Chen ZJ: Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 2015; 347:aaa2630.
171. Abe T, Barber GN: Cytosolic-DNA-mediated, STING-dependent proinflammatory gene induction necessitates canonical NF-B activation through TBK1. J Virol 2014; 88: 5328-5341.
172. Dai P, Wang W, Cao H, Avogadri F, Dai L, Drexler I, Joyce JA, Li XD, Chen Z, Merghoub T, Shuman S, Deng L: Modified vaccinia virus Ankara triggers type I IFN production in murine conventional dendritic cells via a cGAS/STING-mediated cytosolic DNA-sensing pathway. PLoS Pathog 2014; 10:e1003989.
173. Dansako H, Ueda Y, Okumura N, Satoh S, Sugiyama M, Mizokami M, Ikeda M, Kato N: The cyclic GMP-AMP synthetase-STING signaling pathway is required for both the innate immune response against HBV and the suppression of HBV assembly. FEBS J 2016; 283: 144-156.
174. Lam E, Stein S, Falck-Pedersen E: Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade. J Virol 2014; 88: 974-981.
175. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ: Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013; 341: 1390-1394.
176. Wu JJ, Li W, Shao Y, Avey D, Fu B, Gillen J, Hand T, Ma S, Liu X, Miley W, Konrad A, Neipel F, Sturzl M, Whitby D, Li H, Zhu F: Inhibition of cGAS DNA sensing by a herpesvirus virion protein. Cell Host Microbe 2015; 18: 333-344.
177. Collins AC, Cai H, Li T, Franco LH, Li XD, Nair VR, Scharn CR, Stamm CE, Levine B, Chen ZJ, Shiloh MU: Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis . Cell Host Microbe 2015; 17: 820-828.
178. Dey B, Dey RJ, Cheung LS, Pokkali S, Guo H, Lee JH, Bishai WR: A bacterial cyclic dinucleotide activates the cytosolic surveillance pathway and mediates innate resistance to tuberculosis. Nat Med 2015; 21: 401-406.
179. Hansen K, Prabakaran T, Laustsen A, Jorgensen SE, Rahbaek SH, Jensen SB, Nielsen R, Leber JH, Decker T, Horan KA, Jakobsen MR, Paludan SR: Listeria monocytogenes induces IFN expression through an IFI16-, cGAS-and STING-dependent pathway. EMBO J 2014; 33: 1654-1666.
180. Storek KM, Gertsvolf NA, Ohlson MB, Monack DM: cGAS and IFI204 cooperate to produce type I IFNs in response to Francisella infection. J Immunol 2015; 194: 3236-3245.
181. Watson RO, Bell SL, MacDuff DA, Kimmey JM, Diner EJ, Olivas J, Vance RE, Stallings CL, Virgin HW, Cox JS: The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 2015; 17: 811-819.
182. Woodward JJ, Iavarone AT, Portnoy DA: cdi-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 2010; 328: 1703-1705.
183. Zhang Y, Yeruva L, Marinov A, Prantner D, Wyrick PB, Lupashin V, Nagarajan UM: The DNA sensor, cyclic GMP-AMP synthase, is essential for induction of IFN- during Chlamydia trachomatis infection. J Immunol 2014; 193: 2394-2404.
184. Crow YJ, Manel N: Aicardi-Goutieres syndrome and the type I interferonopathies. Nat Rev Immunol 2015; 15: 429-440.
185. Gall A, Treuting P, Elkon KB, Loo YM, Gale M Jr, Barber GN, Stetson DB: Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferondependent autoimmune disease. Immunity 2012; 36: 120-131.
186. Morita M, Stamp G, Robins P, Dulic A, Rosewell I, Hrivnak G, Daly G, Lindahl T, Barnes DE: Gene-targeted mice lacking the Trex1 (DNase III) 3 ->5 DNA exonuclease develop inflammatory myocarditis. Mol Cell Biol 2004; 24: 6719-6727.
187. Stetson DB, Ko JS, Heidmann T, Medzhitov R: Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008; 134: 587-598.
188. Gao D, Li T, Li XD, Chen X, Li QZ, Wight-Carter M, Chen ZJ: Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc Natl Acad Sci USA 2015; 112:E5699-E5705.
189. Gray EE, Treuting PM, Woodward JJ, Stetson DB: Cutting edge: cGAS is required for lethal autoimmune disease in the Trex1-deficient mouse model of Aicardi-Goutieres syndrome. J Immunol 2015; 195: 1939-1943.
190. Kawane K, Fukuyama H, Kondoh G, Takeda J, Ohsawa Y, Uchiyama Y, Nagata S: Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 2001; 292: 1546-1549.
191. Yoshida H, Okabe Y, Kawane K, Fukuyama H, Nagata S: Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat Immunol 2005; 6: 49-56.
192. Kawane K, Ohtani M, Miwa K, Kizawa T, Kanbara Y, Yoshioka Y, Yoshikawa H, Nagata S: Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 2006; 443: 998-1002.
193. Ahn J, Gutman D, Saijo S, Barber GN: STING manifests self DNA-dependent inflammatory disease. Proc Natl Acad Sci USA 2012; 109: 19386-19391.
194. Sharma S, Campbell AM, Chan J, Schattgen SA, Orlowski GM, Nayar R, Huyler AH, Nundel K, Mohan C, Berg LJ, Shlomchik MJ, Marshak-Rothstein A, Fitzgerald KA: Suppression of systemic autoimmunity by the innate immune adaptor STING. Proc Natl Acad Sci USA 2015; 112:E710-E717.
195. Xia P, Ye B, Wang S, Zhu X, Du Y, Xiong Z, Tian Y, Fan Z: Glutamylation of the DNA sensor cGAS regulates its binding and synthase activity in antiviral immunity. Nat Immunol 2016; 17: 369-378.
196. Seo GJ, Yang A, Tan B, Kim S, Liang Q, Choi Y, Yuan W, Feng P, Park HS, Jung JU: AKT kinase-mediated checkpoint of cGAS DNA sensing pathway. Cell Rep 2015; 13: 440-449.
197. Caballero S, Pamer EG: Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol 2015; 33: 227-256.
198. Gensollen T, Iyer SS, Kasper DL, Blumberg RS: How colonization by microbiota in early life shapes the immune system. Science 2016; 352: 539-544.
199. Sonnenberg GF, Artis D: Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease. Immunity 2012; 37: 601-610.
200. Mavrommatis B, Young GR, Kassiotis G: Counterpoise between the microbiome, host immune activation and pathology. Curr Opin Immunol 2013; 25: 456-462.
201. Littman DR, Pamer EG: Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 2011; 10: 311-323.
202. Donia MS, Fischbach MA: Human microbiota. Small molecules from the human microbiota. Science 2015; 349: 1254766.
203. Donaldson GP, Lee SM, Mazmanian SK: Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 2016; 14: 20-32.
204. McKenney PT, Pamer EG: From hype to hope: the gut microbiota in enteric infectious disease. Cell 2015; 163: 1326-1332.
205. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI: Human nutrition, the gut microbiome and the immune system. Nature 2011; 474: 327-336.
206. Salzman NH: The role of the microbiome in immune cell development. Ann Allergy Asthma Immunol 2014; 113: 593-598.
207. Zeevi D, Korem T, Segal E: Talking about cross-talk: the immune system and the microbiome. Genome Biol 2016; 17: 50.
208. Deshmukh HS, Liu Y, Menkiti OR, Mei J, Dai N, O'Leary CE, Oliver PM, Kolls JK, Weiser JN, Worthen GS: The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli k1 sepsis in neonatal mice. Nat Med 2014; 20: 524-530.
209. Niess JH, Reinecker HC: Dendritic cells in the recognition of intestinal microbiota. Cell Microbiol 2006; 8: 558-564.
210. Niess JH, Kurachi K, Go XB, Vyas J, Ploegh HL, Fox JG, Reinecker HC: The intestinal microbiota drives the development of a lamina propria dendritic cell system with intestine specific differentiation. Gastroenterology 2004; 126:A34-A34.
211. Fujiwara D, Wei B, Presley LL, Brewer S, McPherson M, Lewinski MA, Borneman J, Braun J: Systemic control of plasmacytoid dendritic cells by CD8(+) T cells and commensal microbiota. J Immunol 2008; 180: 5843-5852.
212. Fujiwara D, Wei B, McPherson M, Braun J: Commensal microbiota and CD8(+)T cells link to control systemic levels of plasmacytoid dendritic cells. Gastroenterology 2007; 132:A397-A397.
213. Ng SC, Benjamin JL, McCarthy NE, Hedin CRH, Koutsoumpas A, Plamondon S, Price CL, Hart AL, Kamm MA, Forbes A, Knight SC, Lindsay JO, Whelan K, Stagg AJ: Relationship between human intestinal dendritic cells, gut microbiota, and disease activity in Crohn's disease. Inflamm Bowel Dis 2011; 17: 2027-2037.
214. Mueller C, Katepalli M, Steinmeyer S, Jayaraman A, Alaniz R: A role for microbiota metabolites in generation of mucosal dendritic cells. J Immunol 2013; 190: 61-65.
215. Young JA, He TH, Reizis B, Winoto A: Commensal microbiota are required for systemic inflammation triggered by necrotic dendritic cells. Cell Rep 2013; 3: 1932-1944.
216. Ruane D, Chorny A, Lee H, Faith J, Pandey G, Shan M, Simchoni N, Rahman A, Garg A, Weinstein EG, Oropallo M, Gaylord M, Ungaro R, Cunningham-Rundles C, Alexandropoulos K, Mucida D, Merad M, Cerutti A, Mehandru S: Microbiota regulate the ability of lung dendritic cells to induce IgA classswitch recombination and generate protective gastrointestinal immune responses. J Exp Med 2016; 213: 53-73.
217. Han D, Walsh MC, Cejas PJ, Dang NN, Kim YF, Kim J, Charrier-Hisamuddin L, Chau L, Zhang Q, Bittinger K, Bushman FD, Turka LA, Shen H, Reizis B, DeFranco AL, Wu GD, Choi Y: Dendritic cell expression of the signaling molecule TRAF6 is critical for gut microbiota-dependent immune tolerance. Immunity 2013; 38: 1211-1222.
218. Hagerbrand K, Westlund J, Yrlid U, Agace W, Johansson-Lindbom B: Myd88 signaling regulates steady-state migration of intestinal CD103(+) dendritic cells independently of TNF- And the gut microbiota. J Immunol 2015; 195: 2888-2899.
219. Matsuoka K, Sheikh SZ, Li FL, Uno JK, Plevy SE: Macrophage tolerance to the enteric microbiota is mediated by IL-10 at the chromatin level. Gastroenterology 2009; 136:A256-A256.
220. Lopes MM, Carneiro MBH, dos Santos LM, Vaz LG, Martins FD, Vieira LQ: Absence of microbiota impairs macrophage microbicide activity and production of nitric oxide and reative species of oxygen. Free Radical Bio Med 2012; 53:S79-S79.
221. Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BMM, Bailey MT: The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Brain Behav Immun 2012; 26: 371-382.
222. Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S, Sinha R, Mantegazza AR, Ma HL, Crawford A, Angelosanto JM, Wherry EJ, Koni PA, Bushman FD, Elson CO, Eberl G, Artis D, Sonnenberg GF: Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 2013;498:113-117.
223. Sawa S, Lochner M, Satoh-Takayama N, Dulauroy S, Berard M, Kleinschek M, Cua D, Di Santo JP, Eberl G: RORt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 2011; 12:U320-U371.
224. Moro K, Koyasu S: Innate lymphoid cells, possible interaction with microbiota. Semin Immunopathol 2015; 37: 27-37.
225. Guo XH, Liang Y, Zhang Y, Lasorella A, Kee BL, Fu YX: Innate lymphoid cells control early colonization resistance against intestinal pathogens through ID2-dependent regulation of the microbiota. Immunity 2015; 42: 731-743.
226. Buela KAG, Omenetti S, Pizarro TT: Crosstalk between type 3 innate lymphoid cells and the gut microbiota in inflammatory bowel disease. Curr Opin Gastroen 2015; 31: 449-455.
227. Ganal SC, Sanos SL, Kallfass C, Oberle K, Johner C, Kirschning C, Lienenklaus S, Weiss S, Staeheli P, Aichele P, Diefenbach A: Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 2012; 37: 171-186.
228. Chen JN, Wei YF, He JQ, Cui GY, Zhu YN, Lu C, Ding YL, Xue RF, Bai L, Uede T, Li LJ, Diao HY: Natural killer T cells play a necessary role in modulating of immune-mediated liver injury by gut microbiota. Sci Rep 2014; 4: 7259.
229. Chehoud C, Rafail S, Tyldsley AS, Seykora JT, Lambris JD, Grice EA: Complement modulates the cutaneous microbiome and inflammatory milieu. Proc Natl Acad Sci USA 2013; 110: 15061-15066.
230. Salzman NH, Bos NA, Harmsen HJ, Welling GW, Paterson Y, Bevins CL: Regulation of the intestinal microbiota by Paneth cell defensins. Gastroenterology 2005; 128:A508-A508.
231. Salzman NH, Underwood MA, Bevins CL: Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol 2007; 19: 70-83.