Subversion of Cell-Autonomous Host Defense by Chlamydia Infection

  • Annette Fischer
  • Thomas Rudel
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 412)


Obligate intracellular bacteria entirely depend on the metabolites of their host cell for survival and generation of progeny. Due to their lifestyle inside a eukaryotic cell and the lack of any extracellular niche, they have to perfectly adapt to compartmentalized intracellular environment of the host cell and counteract the numerous defense strategies intrinsically present in all eukaryotic cells. This so-called cell-autonomous defense is present in all cell types encountering Chlamydia infection and is in addition closely linked to the cellular innate immune defense of the mammalian host. Cell type and chlamydial species-restricted mechanisms point a long-term evolutionary adaptation that builds the basis of the currently observed host and cell-type tropism among different Chlamydia species. This review will summarize the current knowledge on the strategies pathogenic Chlamydia species have developed to subvert and overcome the multiple mechanisms by which eukaryotic cells defend themselves against intracellular pathogens.



Danger-associated molecular pattern


Guanylate-binding protein


2,3-indoleamine dioxygenase


Immunity-related GTPase


Interferon-stimulated gene


NOD-like receptor


Pathogen-associated molecular pattern


Pattern recognition receptor


Reactive nitrogen species


Reactive oxygen species


Type 3 secretion system


Type 4 secretion system


Toll-like receptor


Uncoordinated 51-like kinase


  1. Abdul-Sater AA, Koo E, Hacker G, Ojcius DM (2009) Inflammasome-dependent caspase-1 activation in cervical epithelial cells stimulates growth of the intracellular pathogen Chlamydia trachomatis. J Biol Chem 284(39):26789–26796. doi: 10.1074/jbc.M109.026823 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abdul-Sater AA, Said-Sadier N, Lam VM, Singh B, Pettengill MA, Soares F, Tattoli I, Lipinski S, Girardin SE, Rosenstiel P, Ojcius DM (2010a) Enhancement of reactive oxygen species production and chlamydial infection by the mitochondrial Nod-like family member NLRX1. J Biol Chem 285(53):41637–41645. doi: 10.1074/jbc.M110.137885 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Abdul-Sater AA, Said-Sadier N, Padilla EV, Ojcius DM (2010b) Chlamydial infection of monocytes stimulates IL-1beta secretion through activation of the NLRP3 inflammasome. Microbes Infect 12(8–9):652–661. doi: 10.1016/j.micinf.2010.04.008 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801. doi: 10.1016/j.cell.2006.02.015 CrossRefPubMedGoogle Scholar
  5. Al-Younes HM, Brinkmann V, Meyer TF (2004) Interaction of Chlamydia trachomatis serovar L2 with the host autophagic pathway. Infect Immun 72(8):4751–4762. doi: 10.1128/IAI.72.8.4751-4762.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Al-Younes HM, Al-Zeer MA, Khalil H, Gussmann J, Karlas A, Machuy N, Brinkmann V, Braun PR, Meyer TF (2011) Autophagy-independent function of MAP-LC3 during intracellular propagation of Chlamydia trachomatis. Autophagy 7(8):814–828CrossRefPubMedGoogle Scholar
  7. Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF (2009) IFN-gamma-inducible Irga6 mediates host resistance against Chlamydia trachomatis via autophagy. PLoS ONE 4(2):e4588. doi: 10.1371/journal.pone.0004588 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Al-Zeer MA, Al-Younes HM, Lauster D, Abu Lubad M, Meyer TF (2013) Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins. Autophagy 9(1):50–62. doi: 10.4161/auto.22482 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ashida H, Mimuro H, Ogawa M, Kobayashi T, Sanada T, Kim M, Sasakawa C (2011) Cell death and infection: a double-edged sword for host and pathogen survival. J Cell Biol 195(6):931–942. doi: 10.1083/jcb.201108081 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Asrat S, de Jesus DA, Hempstead AD, Ramabhadran V, Isberg RR (2014) Bacterial pathogen manipulation of host membrane trafficking. Annu Rev Cell Dev Biol 30:79–109. doi: 10.1146/annurev-cellbio-100913-013439 CrossRefPubMedGoogle Scholar
  11. Bartlett EC, Levison WB, Munday PE (2013) Pelvic inflammatory disease. BMJ 346:f3189. doi: 10.1136/bmj.f3189 CrossRefPubMedGoogle Scholar
  12. Bastidas RJ, Elwell CA, Engel JN, Valdivia RH (2013) Chlamydial intracellular survival strategies. Cold Spring Harb Perspect Med 3(5):a010256. doi: 10.1101/cshperspect.a010256 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Baud D, Greub G (2011) Intracellular bacteria and adverse pregnancy outcomes. Clin Microbiol Infect 17(9):1312–1322. doi: 10.1111/j.1469-0691.2011.03604.x CrossRefPubMedGoogle Scholar
  14. Beagley KW, Huston WM, Hansbro PM, Timms P (2009) Chlamydial infection of immune cells: altered function and implications for disease. Crit Rev Immunol 29(4):275–305CrossRefPubMedGoogle Scholar
  15. Beatty WL, Byrne GI, Morrison RP (1993) Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc Natl Acad Sci U S A 90(9):3998–4002CrossRefPubMedPubMedCentralGoogle Scholar
  16. Beatty WL, Belanger TA, Desai AA, Morrison RP, Byrne GI (1994a) Tryptophan depletion as a mechanism of gamma interferon-mediated chlamydial persistence. Infect Immun 62(9):3705–3711PubMedPubMedCentralGoogle Scholar
  17. Beatty WL, Morrison RP, Byrne GI (1994b) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58(4):686–699PubMedPubMedCentralGoogle Scholar
  18. Bebear C, de Barbeyrac B (2009) Genital Chlamydia trachomatis infections. Clin Microbiol Infect 15(1):4–10. doi: 10.1111/j.1469-0691.2008.02647.x CrossRefPubMedGoogle Scholar
  19. Belland RJ, Scidmore MA, Crane DD, Hogan DM, Whitmire W, McClarty G, Caldwell HD (2001) Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc Natl Acad Sci U S A 98(24):13984–13989. doi: 10.1073/pnas.241377698 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Bergsbaken T, Fink SL, Cookson BT (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7(2):99–109. doi: 10.1038/nrmicro2070 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Bernstein-Hanley I, Coers J, Balsara ZR, Taylor GA, Starnbach MN, Dietrich WF (2006) The p47 GTPases Igtp and Irgb10 map to the Chlamydia trachomatis susceptibility locus Ctrq-3 and mediate cellular resistance in mice. Proc Natl Acad Sci U S A 103(38):14092–14097. doi: 10.1073/pnas.0603338103 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Beug ST, Cheung HH, LaCasse EC, Korneluk RG (2012) Modulation of immune signalling by inhibitors of apoptosis. Trends Immunol 33(11):535–545. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  23. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, Waterman SR, Ryder TA, Boucrot E, Holden DW (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19(13):3235–3249. doi: 10.1093/emboj/19.13.3235 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Bohme L, Rudel T (2009) Host cell death machinery as a target for bacterial pathogens. Microbes Infect 11(13):1063–1070. doi: 10.1016/j.micinf.2009.08.014 CrossRefPubMedGoogle Scholar
  25. Boman J, Hammerschlag MR (2002) Chlamydia pneumoniae and atherosclerosis: critical assessment of diagnostic methods and relevance to treatment studies. Clin Microbiol Rev 15(1):1–20CrossRefPubMedPubMedCentralGoogle Scholar
  26. Broz P, Monack DM (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev 243(1):174–190. doi: 10.1111/j.1600-065X.2011.01041.x CrossRefPubMedPubMedCentralGoogle Scholar
  27. Broz P, Monack DM (2013) Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 13(8):551–565. doi: 10.1038/nri3479 CrossRefPubMedGoogle Scholar
  28. Buchholz KR, Stephens RS (2007) The extracellular signal-regulated kinase/mitogen-activated protein kinase pathway induces the inflammatory factor interleukin-8 following Chlamydia trachomatis infection. Infect Immun 75(12):5924–5929. doi: 10.1128/IAI.01029-07 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Burstein GR, Gaydos CA, Diener-West M, Howell MR, Zenilman JM, Quinn TC (1998) Incident Chlamydia trachomatis infections among inner-city adolescent females. JAMA 280(6):521–526CrossRefPubMedGoogle Scholar
  30. Caldwell HD, Wood H, Crane D, Bailey R, Jones RB, Mabey D, Maclean I, Mohammed Z, Peeling R, Roshick C, Schachter J, Solomon AW, Stamm WE, Suchland RJ, Taylor L, West SK, Quinn TC, Belland RJ, McClarty G (2003) Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J Clin Invest 111(11):1757–1769. doi: 10.1172/JCI17993 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Carlin JM, Weller JB (1995) Potentiation of interferon-mediated inhibition of Chlamydia infection by interleukin-1 in human macrophage cultures. Infect Immun 63(5):1870–1875PubMedPubMedCentralGoogle Scholar
  32. Chen F, Cheng W, Zhang S, Zhong G, Yu P (2010) [Induction of IL-8 by Chlamydia trachomatis through MAPK pathway rather than NF-kappaB pathway]. Zhong nan da xue xue bao Yi xue ban. J Central South Univ Med Sci 35(4):307–313. doi: 10.3969/j.issn.1672-7347.2010.04.005
  33. Chumduri C, Gurumurthy RK, Zadora PK, Mi Y, Meyer TF (2013) Chlamydia infection promotes host DNA damage and proliferation but impairs the DNA damage response. Cell Host Microbe 13(6):746–758. doi: 10.1016/j.chom.2013.05.010 CrossRefPubMedGoogle Scholar
  34. Coccia EM, Battistini A (2015) Early IFN type I response: Learning from microbial evasion strategies. Semin Immunol 27(2):85–101. doi: 10.1016/j.smim.2015.03.005 CrossRefPubMedGoogle Scholar
  35. Coers J, Bernstein-Hanley I, Grotsky D, Parvanova I, Howard JC, Taylor GA, Dietrich WF, Starnbach MN (2008) Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J Immunol 180(9):6237–6245CrossRefPubMedGoogle Scholar
  36. Coombes BK, Mahony JB (2002) Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells. Cell Microbiol 4(7):447–460CrossRefPubMedGoogle Scholar
  37. Cotter TW, Ramsey KH, Miranpuri GS, Poulsen CE, Byrne GI (1997) Dissemination of Chlamydia trachomatis chronic genital tract infection in gamma interferon gene knockout mice. Infect Immun 65(6):2145–2152PubMedPubMedCentralGoogle Scholar
  38. Creasey EA, Isberg RR (2012) The protein SdhA maintains the integrity of the legionella-containing vacuole. Proc Natl Acad Sci U S A 109(9):3481–3486. doi: 10.1073/pnas.1121286109 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Creasey EA, Isberg RR (2014) Maintenance of vacuole integrity by bacterial pathogens. Curr Opin Microbiol 17:46–52. doi: 10.1016/j.mib.2013.11.005 CrossRefPubMedGoogle Scholar
  40. Damiani MT, Gambarte Tudela J, Capmany A (2014) Targeting eukaryotic Rab proteins: a smart strategy for chlamydial survival and replication. Cell Microbiol 16(9):1329–1338. doi: 10.1111/cmi.12325 CrossRefPubMedGoogle Scholar
  41. Darville T, Hiltke TJ (2010) Pathogenesis of genital tract disease due to Chlamydia trachomatis. J Infect Dis 201(Suppl 2):S114–S125CrossRefPubMedPubMedCentralGoogle Scholar
  42. Darville T, O’Neill JM, Andrews CW Jr, Nagarajan UM, Stahl L, Ojcius DM (2003) Toll-like receptor-2, but not Toll-like receptor-4, is essential for development of oviduct pathology in chlamydial genital tract infection. J Immunol 171(11):6187–6197CrossRefPubMedGoogle Scholar
  43. Deretic V, Saitoh T, Akira S (2013) Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13(10):722–737. doi: 10.1038/nri3532 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Eisenreich W, Heesemann J, Rudel T, Goebel W (2013) Metabolic host responses to infection by intracellular bacterial pathogens. Front Cellul Infect Microbiol 3:24. doi: 10.3389/fcimb.2013.00024 CrossRefGoogle Scholar
  45. Fan T, Lu H, Hu H, Shi L, McClarty GA, Nance DM, Greenberg AH, Zhong G (1998) Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med 187(4):487–496CrossRefPubMedPubMedCentralGoogle Scholar
  46. Finethy R, Jorgensen I, Haldar AK, de Zoete MR, Strowig T, Flavell RA, Yamamoto M, Nagarajan UM, Miao EA, Coers J (2015) Guanylate binding proteins enable rapid activation of canonical and noncanonical inflammasomes in chlamydia-infected macrophages. Infect Immun 83(12):4740–4749. doi: 10.1128/IAI.00856-15 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Fischer SF, Harlander T, Vier J, Hacker G (2004) Protection against CD95-induced apoptosis by chlamydial infection at a mitochondrial step. Infect Immun 72(2):1107–1115CrossRefPubMedPubMedCentralGoogle Scholar
  48. Flego D, Bianco M, Quattrini A, Mancini F, Carollo M, Schiavoni I, Ciervo A, Ausiello CM, Fedele G (2013) Chlamydia pneumoniae modulates human monocyte-derived dendritic cells functions driving the induction of a Type 1/Type 17 inflammatory response. Microbes Infect 15(2):105–114. doi: 10.1016/j.micinf.2012.11.004 CrossRefPubMedGoogle Scholar
  49. Flores R, Zhong G (2015) The Chlamydia pneumoniae inclusion membrane protein Cpn 1027 interacts with host cell Wnt signaling pathway regulator cytoplasmic activation/proliferation-associated protein 2 (Caprin2). PLoS ONE 10(5):e0127909. doi: 10.1371/journal.pone.0127909 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Friedman MG, Dvoskin B, Kahane S (2003) Infections with the chlamydia-like microorganism Simkania negevensis, a possible emerging pathogen. Microbes Infect 5(11):1013–1021CrossRefPubMedGoogle Scholar
  51. Galluzzi L, Lopez-Soto A, Kumar S, Kroemer G (2016) Caspases connect cell-death signaling to organismal homeostasis. Immunity 44(2):221–231. doi: 10.1016/j.immuni.2016.01.020 CrossRefPubMedGoogle Scholar
  52. Gao LY, Kwaik YA (2000) The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol 8(7):306–313CrossRefPubMedGoogle Scholar
  53. Gomes LC, Dikic I (2014) Autophagy in antimicrobial immunity. Mol Cell 54(2):224–233. doi: 10.1016/j.molcel.2014.03.009 CrossRefPubMedGoogle Scholar
  54. Gonzalez E, Rother M, Kerr MC, Al-Zeer MA, Abu-Lubad M, Kessler M, Brinkmann V, Loewer A, Meyer TF (2014) Chlamydia infection depends on a functional MDM2-p53 axis. Nat Commun 5:5201. doi: 10.1038/ncomms6201 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Gordon SB, Read RC (2002) Macrophage defences against respiratory tract infections. Br Med Bull 61:45–61CrossRefPubMedGoogle Scholar
  56. Grayston JT, Aldous MB, Easton A, Wang SP, Kuo CC, Campbell LA, Altman J (1993) Evidence that Chlamydia pneumoniae causes pneumonia and bronchitis. J Infect Dis 168(5):1231–1235CrossRefPubMedGoogle Scholar
  57. Green DR, Galluzzi L, Kroemer G (2014) Cell biology. Metabolic control of cell death. Science 345(6203):1250256. doi: 10.1126/science.1250256 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Greenberg D, Banerji A, Friedman MG, Chiu CH, Kahane S (2003) High rate of Simkania negevensis among Canadian inuit infants hospitalized with lower respiratory tract infections. Scand J Infect Dis 35(8):506–508. doi: 10.1080/00365540310014648 CrossRefPubMedGoogle Scholar
  59. Gross O, Poeck H, Bscheider M, Dostert C, Hannesschlager N, Endres S, Hartmann G, Tardivel A, Schweighoffer E, Tybulewicz V, Mocsai A, Tschopp J, Ruland J (2009) Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459(7245):433–436. doi: 10.1038/nature07965 CrossRefPubMedGoogle Scholar
  60. Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126(6):1135–1145. doi: 10.1016/j.cell.2006.07.033 CrossRefPubMedGoogle Scholar
  61. Gyrd-Hansen M, Meier P (2010) IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 10(8):561–574. doi: 10.1038/nrc2889 CrossRefPubMedGoogle Scholar
  62. Hahn DL (1998) Chlamydia pneumoniae and asthma. Thorax 53(12):1095–1096CrossRefPubMedGoogle Scholar
  63. Haldar AK, Saka HA, Piro AS, Dunn JD, Henry SC, Taylor GA, Frickel EM, Valdivia RH, Coers J (2013) IRG and GBP host resistance factors target aberrant, “non-self” vacuoles characterized by the missing of “self” IRGM proteins. PLoS Pathog 9(6):e1003414. doi: 10.1371/journal.ppat.1003414 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Haldar AK, Piro AS, Pilla DM, Yamamoto M, Coers J (2014) The E2-like conjugation enzyme Atg3 promotes binding of IRG and Gbp proteins to Chlamydia- and Toxoplasma-containing vacuoles and host resistance. PLoS ONE 9(1):e86684. doi: 10.1371/journal.pone.0086684 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Haldar AK, Foltz C, Finethy R, Piro AS, Feeley EM, Pilla-Moffett DM, Komatsu M, Frickel EM, Coers J (2015) Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proc Natl Acad Sci U S A 112(41):E5628–E5637. doi: 10.1073/pnas.1515966112 CrossRefPubMedPubMedCentralGoogle Scholar
  66. He X, Mekasha S, Mavrogiorgos N, Fitzgerald KA, Lien E, Ingalls RR (2010) Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J Immunol 184(10):5743–5754. doi: 10.4049/jimmunol.0903937 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Herweg JA, Rudel T (2015) Interaction of Chlamydiae with human macrophages. FEBS J. doi: 10.1111/febs.13609 CrossRefPubMedGoogle Scholar
  68. Itoh R, Murakami I, Chou B, Ishii K, Soejima T, Suzuki T, Hiromatsu K (2014) Chlamydia pneumoniae harness host NLRP3 inflammasome-mediated caspase-1 activation for optimal intracellular growth in murine macrophages. Biochem Biophys Res Commun 452(3):689–694. doi: 10.1016/j.bbrc.2014.08.128 CrossRefPubMedGoogle Scholar
  69. Ivashkiv LB, Donlin LT (2014) Regulation of type I interferon responses. Nat Rev Immunol 14(1):36–49. doi: 10.1038/nri3581 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Jendro MC, Fingerle F, Deutsch T, Liese A, Kohler L, Kuipers JG, Raum E, Martin M, Zeidler H (2004) Chlamydia trachomatis-infected macrophages induce apoptosis of activated T cells by secretion of tumor necrosis factor-alpha in vitro. Med Microbiol Immunol 193(1):45–52. doi: 10.1007/s00430-003-0182-1 CrossRefPubMedGoogle Scholar
  71. Jiang P, Du W, Wang X, Mancuso A, Gao X, Wu M, Yang X (2011) p53 regulates biosynthesis through direct inactivation of glucose-6-phosphate dehydrogenase. Nat Cell Biol 13(3):310–316. doi: 10.1038/ncb2172 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Joseph B, Goebel W (2007) Life of Listeria monocytogenes in the host cells’ cytosol. Microbes Infect 9(10):1188–1195. doi: 10.1016/j.micinf.2007.05.006 CrossRefPubMedGoogle Scholar
  73. Kahlenberg JM, Dubyak GR (2004) Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am J Physiol Cell Physiol 286(5):C1100–C1108. doi: 10.1152/ajpcell.00494.2003 CrossRefPubMedGoogle Scholar
  74. Karunakaran K, Mehlitz A, Rudel T (2011) Evolutionary conservation of infection-induced cell death inhibition among Chlamydiales. PLoS ONE 6(7):e22528. doi: 10.1371/journal.pone.0022528 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Kawai T, Akira S (2006) TLR signaling. Cell Death Differ 13(5):816–825. doi: 10.1038/sj.cdd.4401850 CrossRefPubMedGoogle Scholar
  76. Knittler MR, Sachse K (2015) Chlamydia psittaci: update on an underestimated zoonotic agent. Pathogens and disease 73(1):1–15. doi: 10.1093/femspd/ftu007 CrossRefPubMedGoogle Scholar
  77. Kocab AJ, Duckett CS (2015) Inhibitor of apoptosis proteins as intracellular signaling intermediates. FEBS J. doi: 10.1111/febs.13554 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Kumar Y, Valdivia RH (2009) Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5(6):593–601. doi: 10.1016/j.chom.2009.05.014 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Kumar H, Kawai T, Akira S (2009) Toll-like receptors and innate immunity. Biochem Biophys Res Commun 388(4):621–625. doi: 10.1016/j.bbrc.2009.08.062 CrossRefPubMedGoogle Scholar
  80. Kumar H, Kawai T, Akira S (2011) Pathogen recognition by the innate immune system. Int Rev Immunol 30(1):16–34. doi: 10.3109/08830185.2010.529976 CrossRefPubMedGoogle Scholar
  81. LaCasse EC, Baird S, Korneluk RG, MacKenzie AE (1998) The inhibitors of apoptosis (IAPs) and their emerging role in cancer. Oncogene 17(25):3247–3259. doi: 10.1038/sj.onc.1202569 CrossRefPubMedGoogle Scholar
  82. Lamkanfi M, Dixit VM (2011) Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol 187(2):597–602. doi: 10.4049/jimmunol.1100229 CrossRefPubMedGoogle Scholar
  83. Lamkanfi M, Dixit VM (2014) Mechanisms and functions of inflammasomes. Cell 157(5):1013–1022. doi: 10.1016/j.cell.2014.04.007 CrossRefPubMedGoogle Scholar
  84. Lamkanfi M, Kanneganti TD, Franchi L, Nunez G (2007) Caspase-1 inflammasomes in infection and inflammation. J Leukoc Biol 82(2):220–225. doi: 10.1189/jlb.1206756 CrossRefPubMedGoogle Scholar
  85. Luo JL, Kamata H, Karin M (2005) The anti-death machinery in IKK/NF-kappaB signaling. J Clin Immunol 25(6):541–550. doi: 10.1007/s10875-005-8217-6 CrossRefPubMedGoogle Scholar
  86. MacMicking JD (2012) Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat Rev Immunol 12(5):367–382. doi: 10.1038/nri3210 CrossRefPubMedPubMedCentralGoogle Scholar
  87. McClarty G, Caldwell HD, Nelson DE (2007) Chlamydial interferon gamma immune evasion influences infection tropism. Curr Opin Microbiol 10(1):47–51. doi: 10.1016/j.mib.2006.12.003 CrossRefPubMedGoogle Scholar
  88. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A, Stivala F, Libra M, Basecke J, Evangelisti C, Martelli AM, Franklin RA (2007) Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 1773(8):1263–1284. doi: 10.1016/j.bbamcr.2006.10.001 CrossRefPubMedGoogle Scholar
  89. Mebratu Y, Tesfaigzi Y (2009) How ERK1/2 activation controls cell proliferation and cell death: is subcellular localization the answer? Cell Cycle 8(8):1168–1175CrossRefPubMedPubMedCentralGoogle Scholar
  90. Mehlitz A, Banhart S, Hess S, Selbach M, Meyer TF (2008) Complex kinase requirements for Chlamydia trachomatis Tarp phosphorylation. FEMS Microbiol Lett 289(2):233–240. doi: 10.1111/j.1574-6968.2008.01390.x CrossRefPubMedGoogle Scholar
  91. Meunier E, Broz P (2015) Interferon-inducible GTPases in cell autonomous and innate immunity. Cell Microbiol. doi: 10.1111/cmi.12546 CrossRefPubMedGoogle Scholar
  92. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A 107(7):3076–3080. doi: 10.1073/pnas.0913087107 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Molano M, Meijer CJ, Weiderpass E, Arslan A, Posso H, Franceschi S, Ronderos M, Munoz N, van den Brule AJ (2005) The natural course of Chlamydia trachomatis infection in asymptomatic Colombian women: a 5-year follow-up study. J Infect Dis 191(6):907–916. doi: 10.1086/428287 CrossRefPubMedGoogle Scholar
  94. Moldoveanu T, Follis AV, Kriwacki RW, Green DR (2014) Many players in BCL-2 family affairs. Trends Biochem Sci 39(3):101–111. doi: 10.1016/j.tibs.2013.12.006 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Moulder JW (1991) Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55(1):143–190PubMedPubMedCentralGoogle Scholar
  96. Munoz-Planillo R, Kuffa P, Martinez-Colon G, Smith BL, Rajendiran TM, Nunez G (2013) K(+) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 38(6):1142–1153. doi: 10.1016/j.immuni.2013.05.016 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Nagarajan UM, Sikes JD, Yeruva L, Prantner D (2012) Significant role of IL-1 signaling, but limited role of inflammasome activation, in oviduct pathology during Chlamydia muridarum genital infection. J Immunol 188(6):2866–2875. doi: 10.4049/jimmunol.1103461 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Nathan CF, Murray HW, Wiebe ME, Rubin BY (1983) Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med 158(3):670–689CrossRefPubMedGoogle Scholar
  99. Nelson DE, Virok DP, Wood H, Roshick C, Johnson RM, Whitmire WM, Crane DD, Steele-Mortimer O, Kari L, McClarty G, Caldwell HD (2005) Chlamydial IFN-gamma immune evasion is linked to host infection tropism. Proc Natl Acad Sci U S A 102(30):10658–10663. doi: 10.1073/pnas.0504198102 CrossRefPubMedPubMedCentralGoogle Scholar
  100. O’Connell CM, Ionova IA, Quayle AJ, Visintin A, Ingalls RR (2006) Localization of TLR2 and MyD88 to Chlamydia trachomatis inclusions. Evidence for signaling by intracellular TLR2 during infection with an obligate intracellular pathogen. J Biol Chem 281(3):1652–1659. doi: 10.1074/jbc.M510182200 CrossRefPubMedGoogle Scholar
  101. Olivares-Zavaleta N, Carmody A, Messer R, Whitmire WM, Caldwell HD (2011) Chlamydia pneumoniae inhibits activated human T lymphocyte proliferation by the induction of apoptotic and pyroptotic pathways. J Immunol 186(12):7120–7126. doi: 10.4049/jimmunol.1100393 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Olive AJ, Haff MG, Emanuele MJ, Sack LM, Barker JR, Elledge SJ, Starnbach MN (2014) Chlamydia trachomatis-induced alterations in the host cell proteome are required for intracellular growth. Cell Host Microbe 15(1):113–124. doi: 10.1016/j.chom.2013.12.009 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Oviedo-Boyso J, Bravo-Patino A, Baizabal-Aguirre VM (2014) Collaborative action of Toll-like and NOD-like receptors as modulators of the inflammatory response to pathogenic bacteria. Mediators Inflamm 2014:432785. doi: 10.1155/2014/432785 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Pachikara N, Zhang H, Pan Z, Jin S, Fan H (2009) Productive Chlamydia trachomatis lymphogranuloma venereum 434 infection in cells with augmented or inactivated autophagic activities. FEMS Microbiol Lett 292(2):240–249. doi: 10.1111/j.1574-6968.2009.01494.x CrossRefPubMedPubMedCentralGoogle Scholar
  105. Padberg I, Janssen S, Meyer TF (2013) Chlamydia trachomatis inhibits telomeric DNA damage signaling via transient hTERT upregulation. Int J Med Microbiol 303(8):463–474. doi: 10.1016/j.ijmm.2013.06.001 CrossRefPubMedGoogle Scholar
  106. Paland N, Rajalingam K, Machuy N, Szczepek A, Wehrl W, Rudel T (2006) NF-kappaB and inhibitor of apoptosis proteins are required for apoptosis resistance of epithelial cells persistently infected with Chlamydophila pneumoniae. Cell Microbiol 8(10):1643–1655. doi: 10.1111/j.1462-5822.2006.00739.x CrossRefPubMedGoogle Scholar
  107. Paland N, Bohme L, Gurumurthy RK, Maurer A, Szczepek AJ, Rudel T (2008) Reduced display of tumor necrosis factor receptor I at the host cell surface supports infection with Chlamydia trachomatis. J Biol Chem 283(10):6438–6448. doi: 10.1074/jbc.M708422200 CrossRefPubMedGoogle Scholar
  108. Patel AL, Chen X, Wood ST, Stuart ES, Arcaro KF, Molina DP, Petrovic S, Furdui CM, Tsang AW (2014) Activation of epidermal growth factor receptor is required for Chlamydia trachomatis development. BMC Microbiol 14:277. doi: 10.1186/s12866-014-0277-4 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Perry LL, Feilzer K, Caldwell HD (1997) Immunity to Chlamydia trachomatis is mediated by T helper 1 cells through IFN-gamma-dependent and -independent pathways. J Immunol 158(7):3344–3352PubMedGoogle Scholar
  110. Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, Tschopp J (2007) Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ 14(9):1583–1589. doi: 10.1038/sj.cdd.4402195 CrossRefPubMedGoogle Scholar
  111. Phillips Campbell R, Kintner J, Whittimore J, Schoborg RV (2012) Chlamydia muridarum enters a viable but non-infectious state in amoxicillin-treated BALB/c mice. Microbes Infect 14(13):1177–1185. doi: 10.1016/j.micinf.2012.07.017 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Pilla DM, Hagar JA, Haldar AK, Mason AK, Degrandi D, Pfeffer K, Ernst RK, Yamamoto M, Miao EA, Coers J (2014) Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc Natl Acad Sci U S A 111(16):6046–6051. doi: 10.1073/pnas.1321700111 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Platanias LC (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5(5):375–386. doi: 10.1038/nri1604 CrossRefPubMedGoogle Scholar
  114. Prakash H, Becker D, Bohme L, Albert L, Witzenrath M, Rosseau S, Meyer TF, Rudel T (2009) cIAP-1 controls innate immunity to C. pneumoniae pulmonary infection. PLoS ONE 4(8):e6519. doi: 10.1371/journal.pone.0006519 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Prebeck S, Kirschning C, Durr S, da Costa C, Donath B, Brand K, Redecke V, Wagner H, Miethke T (2001) Predominant role of toll-like receptor 2 versus 4 in Chlamydia pneumoniae-induced activation of dendritic cells. J Immunol 167(6):3316–3323CrossRefPubMedGoogle Scholar
  116. Prusty BK, Bohme L, Bergmann B, Siegl C, Krause E, Mehlitz A, Rudel T (2012) Imbalanced oxidative stress causes chlamydial persistence during non-productive human herpes virus co-infection. PLoS ONE 7(10):e47427. doi: 10.1371/journal.pone.0047427 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Prusty BK, Krohne G, Rudel T (2013) Reactivation of chromosomally integrated human herpesvirus-6 by telomeric circle formation. PLoS Genet 9(12):e1004033. doi: 10.1371/journal.pgen.1004033 CrossRefPubMedPubMedCentralGoogle Scholar
  118. Rajalingam K, Sharma M, Paland N, Hurwitz R, Thieck O, Oswald M, Machuy N, Rudel T (2006) IAP-IAP complexes required for apoptosis resistance of C. trachomatis-infected cells. PLoS Pathog 2(10):e114. doi: 10.1371/journal.ppat.0020114 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Rajalingam K, Sharma M, Lohmann C, Oswald M, Thieck O, Froelich CJ, Rudel T (2008) Mcl-1 is a key regulator of apoptosis resistance in Chlamydia trachomatis-infected cells. PLoS ONE 3(9):e3102. doi: 10.1371/journal.pone.0003102 CrossRefPubMedPubMedCentralGoogle Scholar
  120. Randow F, Youle RJ (2014) Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe 15(4):403–411. doi: 10.1016/j.chom.2014.03.012 CrossRefPubMedPubMedCentralGoogle Scholar
  121. Rasmussen SJ, Eckmann L, Quayle AJ, Shen L, Zhang YX, Anderson DJ, Fierer J, Stephens RS, Kagnoff MF (1997) Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J Clin Invest 99(1):77–87. doi: 10.1172/JCI119136 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF, White O, Hickey EK, Peterson J, Utterback T, Berry K, Bass S, Linher K, Weidman J, Khouri H, Craven B, Bowman C, Dodson R, Gwinn M, Nelson W, DeBoy R, Kolonay J, McClarty G, Salzberg SL, Eisen J, Fraser CM (2000) Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 28(6):1397–1406CrossRefPubMedPubMedCentralGoogle Scholar
  123. Rodel J, Grosse C, Yu H, Wolf K, Otto GP, Liebler-Tenorio E, Forsbach-Birk V, Straube E (2012) Persistent Chlamydia trachomatis infection of HeLa cells mediates apoptosis resistance through a Chlamydia protease-like activity factor-independent mechanism and induces high mobility group box 1 release. Infect Immun 80(1):195–205. doi: 10.1128/IAI.05619-11 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Roshick C, Wood H, Caldwell HD, McClarty G (2006) Comparison of gamma interferon-mediated antichlamydial defense mechanisms in human and mouse cells. Infect Immun 74(1):225–238. doi: 10.1128/IAI.74.1.225-238.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  125. Rottenberg ME, Gigliotti-Rothfuchs A, Wigzell H (2002) The role of IFN-gamma in the outcome of chlamydial infection. Curr Opin Immunol 14(4):444–451CrossRefPubMedGoogle Scholar
  126. Rudel T, Kepp O, Kozjak-Pavlovic V (2010) Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat Rev Microbiol 8(10):693–705. doi: 10.1038/nrmicro2421 CrossRefPubMedGoogle Scholar
  127. Rupp J, Gieffers J, Klinger M, van Zandbergen G, Wrase R, Maass M, Solbach W, Deiwick J, Hellwig-Burgel T (2007) Chlamydia pneumoniae directly interferes with HIF-1alpha stabilization in human host cells. Cell Microbiol 9(9):2181–2191. doi: 10.1111/j.1462-5822.2007.00948.x CrossRefPubMedGoogle Scholar
  128. Sadler AJ, Williams BR (2008) Interferon-inducible antiviral effectors. Nat Rev Immunol 8(7):559–568. doi: 10.1038/nri2314 CrossRefPubMedPubMedCentralGoogle Scholar
  129. Said-Sadier N, Padilla E, Langsley G, Ojcius DM (2010) Aspergillus fumigatus stimulates the NLRP3 inflammasome through a pathway requiring ROS production and the Syk tyrosine kinase. PLoS ONE 5(4):e10008. doi: 10.1371/journal.pone.0010008 CrossRefPubMedPubMedCentralGoogle Scholar
  130. Sanjuan MA, Dillon CP, Tait SW, Moshiach S, Dorsey F, Connell S, Komatsu M, Tanaka K, Cleveland JL, Withoff S, Green DR (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450(7173):1253–1257. doi: 10.1038/nature06421 CrossRefPubMedGoogle Scholar
  131. Sanjuan MA, Milasta S, Green DR (2009) Toll-like receptor signaling in the lysosomal pathways. Immunol Rev 227(1):203–220. doi: 10.1111/j.1600-065X.2008.00732.x CrossRefPubMedGoogle Scholar
  132. Schneider WM, Chevillotte MD, Rice CM (2014) Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 32:513–545. doi: 10.1146/annurev-immunol-032713-120231 CrossRefPubMedPubMedCentralGoogle Scholar
  133. Schroder K, Tschopp J (2010) The inflammasomes. Cell 140(6):821–832. doi: 10.1016/j.cell.2010.01.040 CrossRefPubMedGoogle Scholar
  134. Scidmore MA, Hackstadt T (2001) Mammalian 14-3-3beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol Microbiol 39(6):1638–1650CrossRefPubMedGoogle Scholar
  135. Shamas-Din A, Kale J, Leber B, Andrews DW (2013) Mechanisms of action of Bcl-2 family proteins. Cold Spring Harb Perspect Biol 5(4):a008714. doi: 10.1101/cshperspect.a008714 CrossRefPubMedPubMedCentralGoogle Scholar
  136. Shao W, Yeretssian G, Doiron K, Hussain SN, Saleh M (2007) The caspase-1 digestome identifies the glycolysis pathway as a target during infection and septic shock. J Biol Chem 282(50):36321–36329. doi: 10.1074/jbc.M708182200 CrossRefPubMedGoogle Scholar
  137. Sharma M, Rudel T (2009) Apoptosis resistance in Chlamydia-infected cells: a fate worse than death? FEMS Immunol Med Microbiol 55(2):154–161. doi: 10.1111/j.1574-695X.2008.00515.x CrossRefPubMedGoogle Scholar
  138. Sharma M, Machuy N, Bohme L, Karunakaran K, Maurer AP, Meyer TF, Rudel T (2011) HIF-1alpha is involved in mediating apoptosis resistance to Chlamydia trachomatis-infected cells. Cell Microbiol 13(10):1573–1585. doi: 10.1111/j.1462-5822.2011.01642.x CrossRefPubMedGoogle Scholar
  139. Shenoy AR, Wellington DA, Kumar P, Kassa H, Booth CJ, Cresswell P, MacMicking JD (2012) GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 336(6080):481–485. doi: 10.1126/science.1217141 CrossRefPubMedGoogle Scholar
  140. Shimada K, Crother TR, Karlin J, Chen S, Chiba N, Ramanujan VK, Vergnes L, Ojcius DM, Arditi M (2011) Caspase-1 dependent IL-1beta secretion is critical for host defense in a mouse model of Chlamydia pneumoniae lung infection. PLoS ONE 6(6):e21477. doi: 10.1371/journal.pone.0021477 CrossRefPubMedPubMedCentralGoogle Scholar
  141. Shimada K, Crother TR, Arditi M (2012) Innate immune responses to Chlamydia pneumoniae infection: role of TLRs, NLRs, and the inflammasome. Microbes Infect 14(14):1301–1307. doi: 10.1016/j.micinf.2012.08.004 CrossRefPubMedPubMedCentralGoogle Scholar
  142. Shin S, Brodsky IE (2015) The inflammasome: Learning from bacterial evasion strategies. Semin Immunol 27(2):102–110. doi: 10.1016/j.smim.2015.03.006 CrossRefPubMedGoogle Scholar
  143. Siegl C, Rudel T (2015) Modulation of p53 during bacterial infections. Nat Rev Microbiol 13(12):741–748. doi: 10.1038/nrmicro3537 CrossRefPubMedGoogle Scholar
  144. Siegl C, Prusty BK, Karunakaran K, Wischhusen J, Rudel T (2014) Tumor suppressor p53 alters host cell metabolism to limit Chlamydia trachomatis infection. Cell Rep 9(3):918–929. doi: 10.1016/j.celrep.2014.10.004 CrossRefPubMedGoogle Scholar
  145. Simon S, Hilbi H (2015) Subversion of cell-autonomous immunity and cell migration by Legionella pneumophila effectors. Front Immunol 6:447. doi: 10.3389/fimmu.2015.00447 CrossRefPubMedPubMedCentralGoogle Scholar
  146. Stratton CW, Sriram S (2003) Association of Chlamydia pneumoniae with central nervous system disease. Microbes Infect 5(13):1249–1253CrossRefPubMedGoogle Scholar
  147. Su H, McClarty G, Dong F, Hatch GM, Pan ZK, Zhong G (2004) Activation of Raf/MEK/ERK/cPLA2 signaling pathway is essential for chlamydial acquisition of host glycerophospholipids. J Biol Chem 279(10):9409–9416. doi: 10.1074/jbc.M312008200 CrossRefPubMedGoogle Scholar
  148. Subbarayal P, Karunakaran K, Winkler AC, Rother M, Gonzalez E, Meyer TF, Rudel T (2015) EphrinA2 receptor (EphA2) is an invasion and intracellular signaling receptor for Chlamydia trachomatis. PLoS Pathog 11(4):e1004846. doi: 10.1371/journal.ppat.1004846 CrossRefPubMedPubMedCentralGoogle Scholar
  149. Sun HS, Eng EW, Jeganathan S, Sin AT, Patel PC, Gracey E, Inman RD, Terebiznik MR, Harrison RE (2012) Chlamydia trachomatis vacuole maturation in infected macrophages. J Leukoc Biol 92(4):815–827. doi: 10.1189/jlb.0711336 CrossRefPubMedPubMedCentralGoogle Scholar
  150. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820. doi: 10.1016/j.cell.2010.01.022 CrossRefPubMedGoogle Scholar
  151. Thomas LW, Lam C, Edwards SW (2010) Mcl-1; the molecular regulation of protein function. FEBS Lett 584(14):2981–2989. doi: 10.1016/j.febslet.2010.05.061 CrossRefPubMedGoogle Scholar
  152. Thorpe LM, Yuzugullu H, Zhao JJ (2015) PI3K in cancer: divergent roles of isoforms, modes of activation and therapeutic targeting. Nat Rev Cancer 15(1):7–24. doi: 10.1038/nrc3860 CrossRefPubMedPubMedCentralGoogle Scholar
  153. van Wijk SJ, Fiskin E, Putyrski M, Pampaloni F, Hou J, Wild P, Kensche T, Grecco HE, Bastiaens P, Dikic I (2012) Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol Cell 47(5):797–809. doi: 10.1016/j.molcel.2012.06.017 CrossRefPubMedPubMedCentralGoogle Scholar
  154. Verbeke P, Welter-Stahl L, Ying S, Hansen J, Hacker G, Darville T, Ojcius DM (2006) Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog 2(5):e45. doi: 10.1371/journal.ppat.0020045 CrossRefPubMedPubMedCentralGoogle Scholar
  155. Vergne I, Chua J, Singh SB, Deretic V (2004) Cell biology of mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 20:367–394. doi: 10.1146/annurev.cellbio.20.010403.114015 CrossRefPubMedGoogle Scholar
  156. Wright HR, Turner A, Taylor HR (2008) Trachoma. Lancet 371(9628):1945–1954. doi: 10.1016/S0140-6736(08)60836-3 CrossRefPubMedGoogle Scholar
  157. Yang SC, Hung CF, Aljuffali IA, Fang JY (2015) The roles of the virulence factor IpaB in Shigella spp. in the escape from immune cells and invasion of epithelial cells. Microbiol Res 181:43–51. doi: 10.1016/j.micres.2015.08.006 CrossRefPubMedGoogle Scholar
  158. Ying S, Fischer SF, Pettengill M, Conte D, Paschen SA, Ojcius DM, Hacker G (2006) Characterization of host cell death induced by Chlamydia trachomatis. Infect Immun 74(11):6057–6066. doi: 10.1128/IAI.00760-06 CrossRefPubMedPubMedCentralGoogle Scholar
  159. Ying S, Christian JG, Paschen SA, Hacker G (2008) Chlamydia trachomatis can protect host cells against apoptosis in the absence of cellular Inhibitor of Apoptosis Proteins and Mcl-1. Microbes Infect 10(1):97–101. doi: 10.1016/j.micinf.2007.10.005 CrossRefPubMedGoogle Scholar
  160. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, Xu H, Liu L, Shao F (2011) The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477(7366):596–600. doi: 10.1038/nature10510 CrossRefPubMedGoogle Scholar
  161. Zhou R, Yazdi AS, Menu P, Tschopp J (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469(7329):221–225. doi: 10.1038/nature09663 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Microbiology and BiocenterUniversity of WürzburgWuerzburgGermany

Personalised recommendations