Deletion of FADD in macrophages and granulocytes results in RIP3- and MyD88-dependent systemic inflammation

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Schock, Suruchi N ^a   Young, Jennifer A ^a   He, Tina H ^a   Sun, Yuefang ^a   Winoto, Astar ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ASSOCIATED DEATH DOMAIN PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN KINASE; PROTEIN RIP3; UNCLASSIFIED DRUG; CRE RECOMBINASE; FADD PROTEIN, MOUSE; INTEGRASE; MYD88 PROTEIN, MOUSE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL COUNT; CELL DEATH; CELL POPULATION; CONTROLLED STUDY; DENDRITIC CELL; GRANULOCYTE; IMMUNOCOMPETENT CELL; IMMUNOPATHOGENESIS; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN DEPLETION; PROTEIN FUNCTION; T LYMPHOCYTE; ANIMAL; APOPTOSIS; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; KNOCKOUT MOUSE; MALE; METABOLISM; NECROSIS; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WESTERN BLOTTING;

MUS;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; FEMALE; GRANULOCYTES; INFLAMMATION; INTEGRASES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELOID DIFFERENTIATION FACTOR 88; NECROSIS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84929485512     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124391     Document Type: Article

References (52)

1. Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21: 685-711. PMID: 12615891
2. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K (2010) Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661. doi: 10.1126/science.1178331 PMID: 20133564
3. Farache J, Zigmond E, Shakhar G, Jung S (2013) Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol Cell Biol 91: 232-239. doi: 10.1038/icb.2012.79 PMID: 23399695
4. Galli SJ, Borregaard N, Wynn TA (2011) Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol 12: 1035-1044. doi: 10.1038/ni.2109 PMID: 22012443
5. Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T, et al. (2002) In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17: 211-220. PMID: 12196292
6. Kassim SH, Rajasagi NK, Zhao X, Chervenak R, Jennings SR (2006) 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 80: 3985-3993. PMID: 16571815
7. Chen M, Wang YH, Wang Y, Huang L, Sandoval H, Liu YJ, et al. (2006) Dendritic cell apoptosis in the maintenance of immune tolerance. Science 311: 1160-1164. PMID: 16497935
8. Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, Beighton RA, et al. (2007) Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 26: 629-641. PMID: 17509906
9. Schreiber HA, Loschko J, Karssemeijer RA, Escolano A, Meredith MM, Mucida D, et al. (2013) Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J Exp Med 210: 2025-2039. doi: 10.1084/jem.20130903 PMID: 24043764
10. Goren I, Allmann N, Yogev N, Schurmann C, Linke A, Holdener M, et al. (2009) A transgenic mouse model of inducible macrophage depletion: effects of diphtheria toxin-driven lysozyme M-specific cell lineage ablation on wound inflammatory, angiogenic, and contractive processes. Am J Pathol 175: 132-147. doi: 10.2353/ajpath.2009.081002 PMID: 19528348
11. Fink SL, Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916. PMID: 15784530
12. Duprez L, Wirawan E, Vanden Berghe T, Vandenabeele P (2009) Major cell death pathways at a glance. Microbes Infect 11: 1050-1062. doi: 10.1016/j.micinf.2009.08.013 PMID: 19733681
13. Kepp O, Galluzzi L, Zitvogel L, Kroemer G (2010) Pyroptosis-a cell death modality of its kind? Eur J Immunol 40: 627-630. doi: 10.1002/eji.200940160 PMID: 20201017
14. Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S (2012) Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nature Immunol 13: 954-962. doi: 10.1038/ni.2397 PMID: 22922364
15. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nature Rev Mol Cell Biol 11: 700-714. doi: 10.1038/nrm2970 PMID: 20823910
16. Han J, Zhong CQ, Zhang DW (2011) Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nature Immunol 12: 1143-1149. doi: 10.1038/ni.2159 PMID: 22089220
17. Christofferson DE, Li Y, Yuan J (2014) Control of life-or-death decisions by RIP1 kinase. Annu Rev Physiol 76: 129-150. doi: 10.1146/annurev-physiol-021113-170259 PMID: 24079414
18. Lamkanfi M, Dixit VM (2014) Mechanisms and Functions of Inflammasomes. Cell 157: 1013-1022. doi: 10.1016/j.cell.2014.04.007 PMID: 24855941
19. Chan FK, Luz NF, Moriwaki K (2015) Programmed Necrosis in the Cross Talk of Cell Death and Inflammation. Annu Rev Immunol 33: 4.1-4.28.
20. Pasparakis M, Vandenabeele P (2015) Necroptosis and its role in inflammation. Nature 517: 311-320. doi: 10.1038/nature14191 PMID: 25592536
21. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, et al. (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137: 1112-1123. doi: 10.1016/j.cell.2009.05.037 PMID: 19524513
22. He S, Wang L, Miao L, Wang T, Du F, Zhao L, et al. (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137: 1100-1111. doi: 10.1016/j.cell.2009.05.021 PMID: 19524512
23. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, et al. (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325: 332-336. doi: 10.1126/science.1172308 PMID: 19498109
24. Zhang H, Zhou X, McQuade T, Li J, Chan FK, Zhang J (2011) Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471: 373-376. doi: 10.1038/nature09878 PMID: 21368761
25. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, et al. (2011) Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471: 363-367. doi: 10.1038/nature09852 PMID: 21368763
26. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, et al. (2011) RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471: 368-372. doi: 10.1038/nature09857 PMID: 21368762
27. Chan FK, Shisler J, Bixby JG, Felices M, Zheng L, Appel M, et al. (2003) A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 278: 51613-51621. PMID: 14532286
28. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, et al. (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nature Immunol 1: 489-495. PMID: 11101870
29. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, et al. (2004) Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 279: 10822-10828. PMID: 14701813
30. Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S (1998) Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol 143: 1353-1360. PMID: 9832562
31. Bell BD, Leverrier S, Weist BM, Newton RH, Arechiga AF, Luhrs KA, et al. (2008) FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc Natl Acad Sci USA 105: 16677-16682. doi: 10.1073/pnas.0808597105 PMID: 18946037
32. Ch'en IL, Beisner DR, Degterev A, Lynch C, Yuan J, Hoffmann A, et al. (2008) Antigen-mediated T cell expansion regulated by parallel pathways of death. Proc Natl Acad Sci USA 105: 17463-17468. doi: 10.1073/pnas.0808043105 PMID: 18981423
33. Osborn SL, Diehl GE, Han S-J, Xue L, Kurd N, Hsieh K, et al. (2010) Fas-associated death domain (FADD) is a negative regulator of T-cell receptor-mediated necroptosis. Proc Natl Acad Sci USA 107: 13034-13039. doi: 10.1073/pnas.1005997107 PMID: 20615958
34. Young JA, He TH, Reizis B, Winoto A (2013) Commensal microbiota are required for systemic inflammation triggered by necrotic dendritic cells. Cell Rep 3: 1932-1944. doi: 10.1016/j.celrep.2013.04.033 PMID: 23727238
35. He S, Liang Y, Shao F, Wang X (2011) Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci USA 108: 20054-20059. doi: 10.1073/pnas.1116302108 PMID: 22123964
36. Kaiser WJ, Sridharan H, Huang C, Mandal P, Upton JW, Gough PJ, et al. (2013) Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J Biol Chem 288: 31268-31279. doi: 10.1074/jbc.M113.462341 PMID: 24019532
37. Maelfait J, Vercammen E, Janssens S, Schotte P, Haegman M, Magez S, et al. (2008) Stimulation of Toll-like receptor 3 and 4 induces interleukin-1beta maturation by caspase-8. J Exp Med 205: 1967-1973. doi: 10.1084/jem.20071632 PMID: 18725521
38. Moriwaki K, Bertin J, Gough PJ, Chan FK (2015) A RIPK3-Caspase 8 Complex Mediates Atypical Pro-IL-1beta Processing. J Immunol 194: 1938-1944. doi: 10.4049/jimmunol.1402167 PMID: 25567679
39. Moriwaki K, Balaji S, McQuade T, Malhotra N, Kang J, Chan FK (2014) The necroptosis adaptor RIPK3 promotes injury-induced cytokine expression and tissue repair. Immunity 41: 567-578. doi: 10.1016/j.immuni.2014.09.016 PMID: 25367573
40. Lawlor KE, Khan N, Mildenhall A, Gerlic M, Croker BA, D'Cruz AA, et al. (2015) RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat Commun 6: 6282. doi: 10.1038/ncomms7282 PMID: 25693118
41. Vince JE, Wong WW, Gentle I, Lawlor KE, Allam R, O'Reilly L, et al. (2012) Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36: 215-227. doi: 10.1016/j.immuni.2012.01.012 PMID: 22365665
42. Kang TB, Yang SH, Toth B, Kovalenko A, Wallach D (2013) Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38: 27-40. doi: 10.1016/j.immuni.2012.09.015 PMID: 23260196
43. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150. PMID: 9697844
44. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I (1999) Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265-277. PMID: 10621974
45. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X, et al. (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4: 313-321. doi: 10.1038/nchembio.83 PMID: 18408713
46. Birnberg T, Bar-On L, Sapoznikov A, Caton ML, Cervantes-Barragan L, Makia D, et al. (2008) Lack of conventional dendritic cells is compatible with normal development and T cell homeostasis, but causes myeloid proliferative syndrome. Immunity 29: 986-997. doi: 10.1016/j.immuni.2008.10.012 PMID: 19062318
47. Hochweller K, Miloud T, Striegler J, Naik S, Hammerling GJ, Garbi N (2009) Homeostasis of dendritic cells in lymphoid organs is controlled by regulation of their precursors via a feedback loop. Blood 114: 4411-4421. doi: 10.1182/blood-2008-11-188045 PMID: 19767511
48. McKenna HJ, Stocking KL, Miller RE, Brasel K, De Smedt T, Maraskovsky E, et al. (2000) Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95: 3489-3497. PMID: 10828034
49. Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8: 279-289. doi: 10.1038/nri2215 PMID: 18340345
50. Newton K, Sun X, Dixit VM (2004) Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol Cell Biol 24: 1464-1469. PMID: 14749364
51. Gurung P, Anand PK, Malireddi RK, Vande Walle L, Van Opdenbosch N, Dillon CP, et al. (2014) FADD and caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes. J Immunol 192: 1835-1846. doi: 10.4049/jimmunol.1302839 PMID: 24453255
52. Wang X, Jiang W, Yan Y, Gong T, Han J, Tian Z, et al. (2014) RNA viruses promote activation of the NLRP3 inflammasome through a RIP1-RIP3-DRP1 signaling pathway. Nat Immunol 15: 1126-1133. doi: 10.1038/ni.3015 PMID: 25326752