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The interplay between regulated necrosis and bacterial infection

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Abstract

Necrosis has long been considered as a passive event resulting from a cell extrinsic stimulus, such as pathogen infection. Recent advances have refined this view and it is now well established that necrosis is tightly regulated at the cell level. Regulated necrosis can occur in the context of host–pathogen interactions, and can either participate in the control of infection or favor it. Here, we review the two main pathways implicated so far in bacteria-associated regulated necrosis: caspase 1-dependent pyroptosis and RIPK1/RIPK3-dependent necroptosis. We present how these pathways are modulated in the context of infection by a series of model bacterial pathogens.

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References

  1. Van Praet JT, Donovan E, Vanassche I, Drennan MB, Windels F, Dendooven A, Allais L, Cuvelier CA, van de Loo F, Norris PS, Kruglov AA, Nedospasov SA, Rabot S, Tito R, Raes J, Gaboriau-Routhiau V, Cerf-Bensussan N, Van de Wiele T, Eberl G, Ware CF, Elewaut D (2015) Commensal microbiota influence systemic autoimmune responses. EMBO J 34(4):466–474. doi:10.15252/embj.201489966

    Article  PubMed  PubMed Central  Google Scholar 

  2. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald GF, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O’Toole PW (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184. doi:10.1038/nature11319

    Article  CAS  PubMed  Google Scholar 

  3. Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB, Rhodes JM, Stintzi A, Simpson KW, Hansen JJ, Keku TO, Fodor AA, Jobin C (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338(6103):120–123. doi:10.1126/science.1224820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157(1):121–141. doi:10.1016/j.cell.2014.03.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, Samstein M, Viale A, Socci ND, van den Brink MR, Kamboj M, Pamer EG (2010) Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Investig 120(12):4332–4341. doi:10.1172/JCI43918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, Nomenclature Committee on Cell D (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16(1):3–11. doi:10.1038/cdd.2008.150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Monack DM, Raupach B, Hromockyj AE, Falkow S (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93(18):9833–9838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zychlinsky A, Prevost MC, Sansonetti PJ (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358(6382):167–169. doi:10.1038/358167a0

    Article  CAS  PubMed  Google Scholar 

  10. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, Lipton SA, Lu X, Madeo F, Malorni W, Mehlen P, Nunez G, Peter ME, Piacentini M, Rubinsztein DC, Shi Y, Simon HU, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, Kroemer G (2012) Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 19(1):107–120. doi:10.1038/cdd.2011.96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, Dawson VL (2006) Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 103(48):18314–18319. doi:10.1073/pnas.0606528103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sperandio S, de Belle I, Bredesen DE (2000) An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci 97(26):14376–14381. doi:10.1073/pnas.97.26.14376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B 3rd, Stockwell BR (2012) Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149(5):1060–1072. doi:10.1016/j.cell.2012.03.042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Willingham SB, Bergstralh DT, O’Connor W, Morrison AC, Taxman DJ, Duncan JA, Barnoy S, Venkatesan MM, Flavell RA, Deshmukh M, Hoffman HM, Ting JP (2007) Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2(3):147–159. doi:10.1016/j.chom.2007.07.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J (2005) Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1(2):112–119. doi:10.1038/nchembio711

    Article  CAS  PubMed  Google Scholar 

  16. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 11(10):700–714. doi:10.1038/nrm2970

    Article  CAS  PubMed  Google Scholar 

  17. Galluzzi L, Kepp O, Krautwald S, Kroemer G, Linkermann A (2014) Molecular mechanisms of regulated necrosis. Semin Cell Dev Biol 35:24–32. doi:10.1016/j.semcdb.2014.02.006

    Article  CAS  PubMed  Google Scholar 

  18. Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P (2014) Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 15(2):135–147. doi:10.1038/nrm3737

    Article  CAS  PubMed  Google Scholar 

  19. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J et al (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356(6372):768–774. doi:10.1038/356768a0

    Article  CAS  PubMed  Google Scholar 

  20. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10(2):417–426

    Article  CAS  PubMed  Google Scholar 

  21. Monack DM, Detweiler CS, Falkow S (2001) Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell Microbiol 3(12):825–837

    Article  CAS  PubMed  Google Scholar 

  22. Fink SL, Cookson BT (2006) Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8(11):1812–1825. doi:10.1111/j.1462-5822.2006.00751.x

    Article  CAS  PubMed  Google Scholar 

  23. Carswell EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B (1975) An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci USA 72(9):3666–3670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Laster SM, Wood JG, Gooding LR (1988) Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J Immunol 141(8):2629–2634

    CAS  PubMed  Google Scholar 

  25. Fady C, Gardner A, Jacoby F, Briskin K, Tu Y, Schmid I, Lichtenstein A (1995) Atypical apoptotic cell death induced in L929 targets by exposure to tumor necrosis factor. J Interferon Cytokine Res 15(1):71–80

    Article  CAS  PubMed  Google Scholar 

  26. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1(6):489–495. doi:10.1038/82732

    Article  CAS  PubMed  Google Scholar 

  27. Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114(2):181–190

    Article  CAS  PubMed  Google Scholar 

  28. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137(6):1100–1111. doi:10.1016/j.cell.2009.05.021

    Article  CAS  PubMed  Google Scholar 

  29. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137(6):1112–1123. doi:10.1016/j.cell.2009.05.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325(5938):332–336. doi:10.1126/science.1172308

    Article  CAS  PubMed  Google Scholar 

  31. Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, Wang X (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148(1–2):213–227. doi:10.1016/j.cell.2011.11.031

    Article  CAS  PubMed  Google Scholar 

  32. Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J, Ward Y, Wu LG, Liu ZG (2014) Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 16(1):55–65. doi:10.1038/ncb2883

    Article  CAS  PubMed  Google Scholar 

  33. Chen X, Li W, Ren J, Huang D, He WT, Song Y, Yang C, Li W, Zheng X, Chen P, Han J (2014) Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res 24(1):105–121. doi:10.1038/cr.2013.171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF, Wang FS, Wang X (2014) Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell 54(1):133–146. doi:10.1016/j.molcel.2014.03.003

    Article  CAS  PubMed  Google Scholar 

  35. Clay H, Volkman HE, Ramakrishnan L (2008) Tumor necrosis factor signaling mediates resistance to mycobacteria by inhibiting bacterial growth and macrophage death. Immunity 29(2):283–294. doi:10.1016/j.immuni.2008.06.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Roca FJ, Ramakrishnan L (2013) TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 153(3):521–534. doi:10.1016/j.cell.2013.03.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Clay H, Davis JM, Beery D, Huttenlocher A, Lyons SE, Ramakrishnan L (2007) Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2(1):29–39. doi:10.1016/j.chom.2007.06.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ulrichs T, Kosmiadi GA, Trusov V, Jorg S, Pradl L, Titukhina M, Mishenko V, Gushina N, Kaufmann SH (2004) Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung. J Pathol 204(2):217–228. doi:10.1002/path.1628

    Article  PubMed  Google Scholar 

  39. Davis JM, Ramakrishnan L (2009) The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136(1):37–49. doi:10.1016/j.cell.2008.11.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 17(1):7–15. doi:10.3201/eid1701.091101p1

    Article  PubMed  PubMed Central  Google Scholar 

  41. Richter-Dahlfors A, Buchan AM, Finlay BB (1997) Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186(4):569–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96(5):2396–2401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kim JM, Eckmann L, Savidge TC, Lowe DC, Witthoft T, Kagnoff MF (1998) Apoptosis of human intestinal epithelial cells after bacterial invasion. J Clin Investig 102(10):1815–1823. doi:10.1172/JCI2466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38(1):31–40

    Article  CAS  PubMed  Google Scholar 

  45. Lara-Tejero M, Sutterwala FS, Ogura Y, Grant EP, Bertin J, Coyle AJ, Flavell RA, Galan JE (2006) Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 203(6):1407–1412. doi:10.1084/jem.20060206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Raupach B, Peuschel SK, Monack DM, Zychlinsky A (2006) Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect Immun 74(8):4922–4926. doi:10.1128/IAI.00417-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, Sarkar A, Warren SE, Wewers MD, Aderem A (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11(12):1136–1142. doi:10.1038/ni.1960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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 (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479(7371):117–121. doi:10.1038/nature10558

    Article  CAS  PubMed  Google Scholar 

  49. Broz P, Ruby T, Belhocine K, Bouley DM, Kayagaki N, Dixit VM, Monack DM (2012) Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490(7419):288–291. doi:10.1038/nature11419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Aachoui Y, Leaf IA, Hagar JA, Fontana MF, Campos CG, Zak DE, Tan MH, Cotter PA, Vance RE, Aderem A, Miao EA (2013) Caspase-11 protects against bacteria that escape the vacuole. Science 339(6122):975–978. doi:10.1126/science.1230751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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. Nat Immunol 13(10):954–962. doi:10.1038/ni.2397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Gaillard JL, Berche P, Mounier J, Richard S, Sansonetti P (1987) In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun 55(11):2822–2829

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Vazquez MA, Sicher SC, Wright WJ, Proctor ML, Schmalzried SR, Stallworth KR, Crowley JC, Lu CY (1995) Differential regulation of TNF-alpha production by listeriolysin-producing versus nonproducing strains of Listeria monocytogenes. J Leukoc Biol 58(5):556–562

    CAS  PubMed  Google Scholar 

  54. Kayal S, Lilienbaum A, Poyart C, Memet S, Israel A, Berche P (1999) Listeriolysin O-dependent activation of endothelial cells during infection with Listeria monocytogenes: activation of NF-kappa B and upregulation of adhesion molecules and chemokines. Mol Microbiol 31(6):1709–1722

    Article  CAS  PubMed  Google Scholar 

  55. Carrero JA, Calderon B, Unanue ER (2004) Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J Immunol 172(8):4866–4874

    Article  CAS  PubMed  Google Scholar 

  56. Gonzalez-Juarbe N, Gilley RP, Hinojosa CA, Bradley KM, Kamei A, Gao G, Dube PH, Bergman MA, Orihuela CJ (2015) Pore-forming toxins induce macrophage necroptosis during acute bacterial Pneumonia. PLoS Pathog 11(12):e1005337. doi:10.1371/journal.ppat.1005337

    Article  PubMed  PubMed Central  Google Scholar 

  57. Barsig J, Kaufmann SH (1997) The mechanism of cell death in Listeria monocytogenes-infected murine macrophages is distinct from apoptosis. Infect Immun 65(10):4075–4081

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Cervantes J, Nagata T, Uchijima M, Shibata K, Koide Y (2008) Intracytosolic Listeria monocytogenes induces cell death through caspase-1 activation in murine macrophages. Cell Microbiol 10(1):41–52. doi:10.1111/j.1462-5822.2007.01012.x

    CAS  PubMed  Google Scholar 

  59. Bleriot C, Dupuis T, Jouvion G, Eberl G, Disson O, Lecuit M (2015) Liver-resident macrophage necroptosis orchestrates type 1 microbicidal inflammation and type-2-mediated tissue repair during bacterial infection. Immunity 42(1):145–158. doi:10.1016/j.immuni.2014.12.020

    Article  CAS  PubMed  Google Scholar 

  60. Di Paolo NC, Doronin K, Baldwin LK, Papayannopoulou T, Shayakhmetov DM (2013) The transcription factor IRF3 triggers “defensive suicide” necrosis in response to viral and bacterial pathogens. Cell reports 3(6):1840–1846. doi:10.1016/j.celrep.2013.05.025

    Article  PubMed  PubMed Central  Google Scholar 

  61. Stockinger S, Materna T, Stoiber D, Bayr L, Steinborn R, Kolbe T, Unger H, Chakraborty T, Levy DE, Muller M, Decker T (2002) Production of type I IFN sensitizes macrophages to cell death induced by Listeria monocytogenes. J Immunol 169(11):6522–6529

    Article  CAS  PubMed  Google Scholar 

  62. O’Connell RM, Saha SK, Vaidya SA, Bruhn KW, Miranda GA, Zarnegar B, Perry AK, Nguyen BO, Lane TF, Taniguchi T, Miller JF, Cheng G (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200(4):437–445. doi:10.1084/jem.20040712

    Article  PubMed  PubMed Central  Google Scholar 

  63. Auerbuch V, Brockstedt DG, Meyer-Morse N, O’Riordan M, Portnoy DA (2004) Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med 200(4):527–533. doi:10.1084/jem.20040976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Carrero JA, Calderon B, Unanue ER (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 200(4):535–540. doi:10.1084/jem.20040769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Solodova E, Jablonska J, Weiss S, Lienenklaus S (2011) Production of IFN-beta during Listeria monocytogenes infection is restricted to monocyte/macrophage lineage. PLoS One 6(4):e18543. doi:10.1371/journal.pone.0018543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. White DW, Harty JT (1998) Perforin-deficient CD8+ T cells provide immunity to Listeria monocytogenes by a mechanism that is independent of CD95 and IFN-gamma but requires TNF-alpha. J Immunol 160(2):898–905

    CAS  PubMed  Google Scholar 

  67. Wassef JS, Keren DF, Mailloux JL (1989) Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 57(3):858–863

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Zychlinsky A, Thirumalai K, Arondel J, Cantey JR, Aliprantis AO, Sansonetti PJ (1996) In vivo apoptosis in Shigella flexneri infections. Infect Immun 64(12):5357–5365

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Sansonetti PJ, Phalipon A, Arondel J, Thirumalai K, Banerjee S, Akira S, Takeda K, Zychlinsky A (2000) Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12(5):581–590

    Article  CAS  PubMed  Google Scholar 

  70. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303(5663):1532–1535. doi:10.1126/science.1092385

    Article  CAS  PubMed  Google Scholar 

  71. Carneiro LA, Travassos LH, Soares F, Tattoli I, Magalhaes JG, Bozza MT, Plotkowski MC, Sansonetti PJ, Molkentin JD, Philpott DJ, Girardin SE (2009) Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5(2):123–136. doi:10.1016/j.chom.2008.12.011

    Article  CAS  PubMed  Google Scholar 

  72. Bergounioux J, Elisee R, Prunier AL, Donnadieu F, Sperandio B, Sansonetti P, Arbibe L (2012) Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium’s epithelial niche. Cell Host Microbe 11(3):240–252. doi:10.1016/j.chom.2012.01.013

    Article  CAS  PubMed  Google Scholar 

  73. Kobayashi T, Ogawa M, Sanada T, Mimuro H, Kim M, Ashida H, Akakura R, Yoshida M, Kawalec M, Reichhart JM, Mizushima T, Sasakawa C (2013) The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection. Cell Host Microbe 13(5):570–583. doi:10.1016/j.chom.2013.04.012

    Article  CAS  PubMed  Google Scholar 

  74. Hanski C, Kutschka U, Schmoranzer HP, Naumann M, Stallmach A, Hahn H, Menge H, Riecken EO (1989) Immunohistochemical and electron microscopic study of interaction of Yersinia enterocolitica serotype O8 with intestinal mucosa during experimental enteritis. Infect Immun 57(3):673–678

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Autenrieth IB, Firsching R (1996) Penetration of M cells and destruction of Peyer’s patches by Yersinia enterocolitica: an ultrastructural and histological study. J Med Microbiol 44(4):285–294. doi:10.1099/00222615-44-4-285

    Article  CAS  PubMed  Google Scholar 

  76. Marra A, Isberg RR (1997) Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer’s patch intestinal epithelium. Infect Immun 65(8):3412–3421

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Monack DM, Mecsas J, Ghori N, Falkow S (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci USA 94(19):10385–10390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Mills SD, Boland A, Sory MP, van der Smissen P, Kerbourch C, Finlay BB, Cornelis GR (1997) Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc Natl Acad Sci USA 94(23):12638–12643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Bergsbaken T, Cookson BT (2007) Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog 3(11):e161. doi:10.1371/journal.ppat.0030161

    Article  PubMed  PubMed Central  Google Scholar 

  80. Monack DM, Mecsas J, Bouley D, Falkow S (1998) Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J Exp Med 188(11):2127–2137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Brodsky IE, Medzhitov R (2008) Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog 4(5):e1000067. doi:10.1371/journal.ppat.1000067

    Article  PubMed  PubMed Central  Google Scholar 

  82. Zauberman A, Tidhar A, Levy Y, Bar-Haim E, Halperin G, Flashner Y, Cohen S, Shafferman A, Mamroud E (2009) Yersinia pestis endowed with increased cytotoxicity is avirulent in a bubonic plague model and induces rapid protection against pneumonic plague. PLoS One 4(6):e5938. doi:10.1371/journal.pone.0005938

    Article  PubMed  PubMed Central  Google Scholar 

  83. Radin JN, Gonzalez-Rivera C, Ivie SE, McClain MS, Cover TL (2011) Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect Immun 79(7):2535–2543. doi:10.1128/IAI.01370-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kennedy CL, Smith DJ, Lyras D, Chakravorty A, Rood JI (2009) Programmed cellular necrosis mediated by the pore-forming alpha-toxin from Clostridium septicum. PLoS Pathog 5(7):e1000516. doi:10.1371/journal.ppat.1000516

    Article  PubMed  PubMed Central  Google Scholar 

  85. Autheman D, Wyder M, Popoff M, D’Herde K, Christen S, Posthaus H (2013) Clostridium perfringens beta-toxin induces necrostatin-inhibitable, calpain-dependent necrosis in primary porcine endothelial cells. PLoS One 8(5):e64644. doi:10.1371/journal.pone.0064644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Schaale K, Peters KM, Murthy AM, Fritzsche AK, Phan MD, Totsika M, Robertson AA, Nichols KB, Cooper MA, Stacey KJ, Ulett GC, Schroder K, Schembri MA, Sweet MJ (2015) Strain- and host species-specific inflammasome activation, IL-1beta release, and cell death in macrophages infected with uropathogenic Escherichia coli. Mucosal Immunol. doi:10.1038/mi.2015.44

    PubMed  Google Scholar 

  87. Accarias S, Lugo-Villarino G, Foucras G, Neyrolles O, Boullier S, Tabouret G (2015) Pyroptosis of resident macrophages differentially orchestrates inflammatory responses to Staphylococcus aureus in resistant and susceptible mice. Eur J Immunol 45(3):794–806. doi:10.1002/eji.201445098

    Article  CAS  PubMed  Google Scholar 

  88. Kitur K, Parker D, Nieto P, Ahn DS, Cohen TS, Chung S, Wachtel S, Bueno S, Prince A (2015) Toxin-induced necroptosis is a major mechanism of Staphylococcus aureus lung damage. PLoS Pathog 11(4):e1004820. doi:10.1371/journal.ppat.1004820

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We apologize to the many colleagues whose work has not been discussed. We thank the members of the Biology of Infection Unit for helpful discussions. Research in the Biology of Infection Unit is supported by Institut Pasteur, Institut National de la Santé et de la Recherche Médicale, Agence Nationale de la Recherche, LabEx IBEID, the Proantilis EU program and the European Research Council.

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Correspondence to Marc Lecuit.

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Blériot, C., Lecuit, M. The interplay between regulated necrosis and bacterial infection. Cell. Mol. Life Sci. 73, 2369–2378 (2016). https://doi.org/10.1007/s00018-016-2206-1

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  • DOI: https://doi.org/10.1007/s00018-016-2206-1

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