pp 1-26 | Cite as

Subversion of Cell-Autonomous Host Defense by Chlamydia Infection

Chapter
Part of the Current Topics in Microbiology and Immunology book series

Abstract

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.

Abbreviations

DAMP

Danger-associated molecular pattern

GBP

Guanylate-binding protein

IDO

2,3-indoleamine dioxygenase

IRG

Immunity-related GTPase

ISG

Interferon-stimulated gene

NLR

NOD-like receptor

PAMP

Pathogen-associated molecular pattern

PRR

Pattern recognition receptor

RNS

Reactive nitrogen species

ROS

Reactive oxygen species

T3SS

Type 3 secretion system

T4SS

Type 4 secretion system

TLR

Toll-like receptor

ULK

Uncoordinated 51-like kinase

References

  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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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):814–828Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle Scholar
  11. Bartlett EC, Levison WB, Munday PE (2013) Pelvic inflammatory disease. BMJ 346:f3189. doi: 10.1136/bmj.f3189 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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):275–305Google 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):3998–4002Google 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):3705–3711Google Scholar
  17. Beatty WL, Morrison RP, Byrne GI (1994b) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58(4):686–699Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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/j.it.2012.06.004 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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):1–20Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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):521–526Google 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 CrossRefGoogle 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):1870–1875Google 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 CrossRefGoogle 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 CrossRefGoogle 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):6237–6245Google 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):447–460Google 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):2145–2152Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle Scholar
  41. Darville T, Hiltke TJ (2010) Pathogenesis of genital tract disease due to Chlamydia trachomatis. J Infect Dis 201(Suppl 2):S114–S125Google 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):6187–6197Google 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 CrossRefGoogle 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):487–496Google 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 CrossRefGoogle 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):1107–1115Google 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 CrossRefGoogle 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 CrossRefGoogle 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):1013–1021Google 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 CrossRefGoogle Scholar
  52. Gao LY, Kwaik YA (2000) The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol 8(7):306–313Google 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 CrossRefGoogle 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 CrossRefGoogle Scholar
  55. Gordon SB, Read RC (2002) Macrophage defences against respiratory tract infections. Br Med Bull 61:45–61Google 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):1231–1235Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle Scholar
  62. Hahn DL (1998) Chlamydia pneumoniae and asthma. Thorax 53(12):1095–1096Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle Scholar
  67. Herweg JA, Rudel T (2015) Interaction of Chlamydiae with human macrophages. FEBS J. doi: 10.1111/febs.13609 CrossRefGoogle 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 CrossRefGoogle Scholar
  69. IvashkivLB,DonlinLT(2014)RegulationoftypeIinterferonresponses.NatRevImmunol14(1):36–49.doi: 10.1038/nri3581 CrossRefGoogle Scholar
  70. JendroMC,FingerleF,DeutschT,LieseA,KohlerL,KuipersJG,RaumE,MartinM,ZeidlerH(2004)Chlamydiatrachomatis-infectedmacrophagesinduceapoptosisofactivatedTcellsbysecretionoftumornecrosisfactor-alphainvitro.MedMicrobiolImmunol193(1):45–52.doi: 10.1007/s00430-003-0182-1 CrossRefGoogle Scholar
  71. JiangP,DuW,WangX,MancusoA,GaoX,WuM,YangX(2011)p53regulatesbiosynthesisthroughdirectinactivationofglucose-6-phosphatedehydrogenase.NatCellBiol13(3):310–316.doi: 10.1038/ncb2172 CrossRefGoogle Scholar
  72. JosephB,GoebelW(2007)LifeofListeriamonocytogenesinthehostcells’cytosol.MicrobesInfect9(10):1188–1195.doi: 10.1016/j.micinf.2007.05.006 CrossRefGoogle Scholar
  73. KahlenbergJM,DubyakGR(2004)Mechanismsofcaspase-1activationbyP2X7receptor-mediatedK+release.AmJPhysiolCellPhysiol286(5):C1100–C1108.doi: 10.1152/ajpcell.00494.2003 CrossRefGoogle Scholar
  74. KarunakaranK,MehlitzA,RudelT(2011)Evolutionaryconservationofinfection-inducedcelldeathinhibitionamongChlamydiales.PLoSONE6(7):e22528.doi: 10.1371/journal.pone.0022528 CrossRefGoogle Scholar
  75. KawaiT,AkiraS(2006)TLRsignaling.CellDeathDiffer13(5):816–825.doi: 10.1038/sj.cdd.4401850 CrossRefGoogle Scholar
  76. KnittlerMR,SachseK(2015)Chlamydiapsittaci:updateonanunderestimatedzoonoticagent.Pathogensanddisease73(1):1–15.doi: 10.1093/femspd/ftu007 CrossRefGoogle Scholar
  77. KocabAJ,DuckettCS(2015)Inhibitorofapoptosisproteinsasintracellularsignalingintermediates.FEBSJ.doi: 10.1111/febs.13554 CrossRefGoogle Scholar
  78. KumarY,ValdiviaRH(2009)Leadingashelteredlife:intracellularpathogensandmaintenanceofvacuolarcompartments.CellHostMicrobe5(6):593–601.doi: 10.1016/j.chom.2009.05.014 CrossRefGoogle Scholar
  79. KumarH,KawaiT,AkiraS(2009)Toll-likereceptorsandinnateimmunity.BiochemBiophysResCommun388(4):621–625.doi: 10.1016/j.bbrc.2009.08.062 CrossRefGoogle Scholar
  80. KumarH,KawaiT,AkiraS(2011)Pathogenrecognitionbytheinnateimmunesystem.IntRevImmunol30(1):16–34.doi: 10.3109/08830185.2010.529976 CrossRefGoogle Scholar
  81. LaCasseEC,BairdS,KornelukRG,MacKenzieAE(1998)Theinhibitorsofapoptosis(IAPs)andtheiremergingroleincancer.Oncogene17(25):3247–3259.doi: 10.1038/sj.onc.1202569 CrossRefGoogle Scholar
  82. LamkanfiM,DixitVM(2011)Modulationofinflammasomepathwaysbybacterialandviralpathogens.JImmunol187(2):597–602.doi: 10.4049/jimmunol.1100229 CrossRefGoogle Scholar
  83. LamkanfiM,DixitVM(2014)Mechanismsandfunctionsofinflammasomes.Cell157(5):1013–1022.doi: 10.1016/j.cell.2014.04.007 CrossRefGoogle Scholar
  84. LamkanfiM,KannegantiTD,FranchiL,NunezG(2007)Caspase-1inflammasomesininfectionandinflammation.JLeukocBiol82(2):220–225.doi: 10.1189/jlb.1206756 CrossRefGoogle Scholar
  85. LuoJL,KamataH,KarinM(2005)Theanti-deathmachineryinIKK/NF-kappaBsignaling.JClinImmunol25(6):541–550.doi: 10.1007/s10875-005-8217-6 CrossRefGoogle Scholar
  86. MacMickingJD(2012)Interferon-inducibleeffectormechanismsincell-autonomousimmunity.NatRevImmunol12(5):367–382.doi: 10.1038/nri3210 CrossRefGoogle Scholar
  87. McClartyG,CaldwellHD,NelsonDE(2007)Chlamydialinterferongammaimmuneevasioninfluencesinfectiontropism.CurrOpinMicrobiol10(1):47–51.doi: 10.1016/j.mib.2006.12.003 CrossRefGoogle Scholar
  88. McCubreyJA,SteelmanLS,ChappellWH,AbramsSL,WongEW,ChangF,LehmannB,TerrianDM,MilellaM,TafuriA,StivalaF,LibraM,BaseckeJ,EvangelistiC,MartelliAM,FranklinRA(2007)RolesoftheRaf/MEK/ERKpathwayincellgrowth,malignanttransformationanddrugresistance.BiochimBiophysActa1773(8):1263–1284.doi: 10.1016/j.bbamcr.2006.10.001 CrossRefGoogle Scholar
  89. MebratuY,TesfaigziY(2009)HowERK1/2activationcontrolscellproliferationandcelldeath:issubcellularlocalizationtheanswer?CellCycle8(8):1168–1175Google Scholar
  90. MehlitzA,BanhartS,HessS,SelbachM,MeyerTF(2008)ComplexkinaserequirementsforChlamydiatrachomatisTarpphosphorylation.FEMSMicrobiolLett289(2):233–240.doi: 10.1111/j.1574-6968.2008.01390.x CrossRefGoogle Scholar
  91. MeunierE,BrozP(2015)Interferon-inducibleGTPasesincellautonomousandinnateimmunity.CellMicrobiol.doi: 10.1111/cmi.12546 CrossRefGoogle Scholar
  92. MiaoEA,MaoDP,YudkovskyN,BonneauR,LorangCG,WarrenSE,LeafIA,AderemA(2010)InnateimmunedetectionofthetypeIIIsecretionapparatusthroughtheNLRC4inflammasome.ProcNatlAcadSciUSA107(7):3076–3080.doi: 10.1073/pnas.0913087107 CrossRefGoogle Scholar
  93. MolanoM,MeijerCJ,WeiderpassE,ArslanA,PossoH,FranceschiS,RonderosM,MunozN,vandenBruleAJ(2005)ThenaturalcourseofChlamydiatrachomatisinfectioninasymptomaticColombianwomen:a5-yearfollow-upstudy.JInfectDis191(6):907–916.doi: 10.1086/428287 CrossRefGoogle Scholar
  94. MoldoveanuT,FollisAV,KriwackiRW,GreenDR(2014)ManyplayersinBCL-2familyaffairs.TrendsBiochemSci39(3):101–111.doi: 10.1016/j.tibs.2013.12.006 CrossRefGoogle Scholar
  95. MoulderJW(1991)Interactionofchlamydiaeandhostcellsinvitro.MicrobiolRev55(1):143–190Google Scholar
  96. Munoz-PlanilloR,KuffaP,Martinez-ColonG,SmithBL,RajendiranTM,NunezG(2013)K(+)effluxisthecommontriggerofNLRP3inflammasomeactivationbybacterialtoxinsandparticulatematter.Immunity38(6):1142–1153.doi: 10.1016/j.immuni.2013.05.016 CrossRefGoogle Scholar
  97. NagarajanUM,SikesJD,YeruvaL,PrantnerD(2012)SignificantroleofIL-1signaling,butlimitedroleofinflammasomeactivation,inoviductpathologyduringChlamydiamuridarumgenitalinfection.JImmunol188(6):2866–2875.doi: 10.4049/jimmunol.1103461 CrossRefGoogle Scholar
  98. NathanCF,MurrayHW,WiebeME,RubinBY(1983)Identificationofinterferon-gammaasthelymphokinethatactivateshumanmacrophageoxidativemetabolismandantimicrobialactivity.JExpMed158(3):670–689Google Scholar
  99. NelsonDE,VirokDP,WoodH,RoshickC,JohnsonRM,WhitmireWM,CraneDD,Steele-MortimerO,KariL,McClartyG,CaldwellHD(2005)ChlamydialIFN-gammaimmuneevasionislinkedtohostinfectiontropism.ProcNatlAcadSciUSA102(30):10658–10663.doi: 10.1073/pnas.0504198102 CrossRefGoogle Scholar
  100. O’ConnellCM,IonovaIA,QuayleAJ,VisintinA,IngallsRR(2006)LocalizationofTLR2andMyD88toChlamydiatrachomatisinclusions.EvidenceforsignalingbyintracellularTLR2duringinfectionwithanobligateintracellularpathogen.JBiolChem281(3):1652–1659.doi: 10.1074/jbc.M510182200 CrossRefGoogle Scholar
  101. Olivares-ZavaletaN,CarmodyA,MesserR,WhitmireWM,CaldwellHD(2011)ChlamydiapneumoniaeinhibitsactivatedhumanTlymphocyteproliferationbytheinductionofapoptoticandpyroptoticpathways.JImmunol186(12):7120–7126.doi: 10.4049/jimmunol.1100393 CrossRefGoogle Scholar
  102. OliveAJ,HaffMG,EmanueleMJ,SackLM,BarkerJR,ElledgeSJ,StarnbachMN(2014)Chlamydiatrachomatis-inducedalterationsinthehostcellproteomearerequiredforintracellulargrowth.CellHostMicrobe15(1):113–124.doi: 10.1016/j.chom.2013.12.009 CrossRefGoogle Scholar
  103. Oviedo-BoysoJ,Bravo-PatinoA,Baizabal-AguirreVM(2014)CollaborativeactionofToll-likeandNOD-likereceptorsasmodulatorsoftheinflammatoryresponsetopathogenicbacteria.MediatorsInflamm2014:432785.doi: 10.1155/2014/432785 CrossRefGoogle Scholar
  104. PachikaraN,ZhangH,PanZ,JinS,FanH(2009)ProductiveChlamydiatrachomatislymphogranulomavenereum434infectionincellswithaugmentedorinactivatedautophagicactivities.FEMSMicrobiolLett292(2):240–249.doi: 10.1111/j.1574-6968.2009.01494.x CrossRefGoogle Scholar
  105. PadbergI,JanssenS,MeyerTF(2013)ChlamydiatrachomatisinhibitstelomericDNAdamagesignalingviatransienthTERTupregulation.IntJMedMicrobiol303(8):463–474.doi: 10.1016/j.ijmm.2013.06.001 CrossRefGoogle Scholar
  106. PalandN,RajalingamK,MachuyN,SzczepekA,WehrlW,RudelT(2006)NF-kappaBandinhibitorofapoptosisproteinsarerequiredforapoptosisresistanceofepithelialcellspersistentlyinfectedwithChlamydophilapneumoniae.CellMicrobiol8(10):1643–1655.doi: 10.1111/j.1462-5822.2006.00739.x CrossRefGoogle Scholar
  107. PalandN,BohmeL,GurumurthyRK,MaurerA,SzczepekAJ,RudelT(2008)ReduceddisplayoftumornecrosisfactorreceptorIatthehostcellsurfacesupportsinfectionwithChlamydiatrachomatis.JBiolChem283(10):6438–6448.doi: 10.1074/jbc.M708422200 CrossRefGoogle Scholar
  108. PatelAL,ChenX,WoodST,StuartES,ArcaroKF,MolinaDP,PetrovicS,FurduiCM,TsangAW(2014)ActivationofepidermalgrowthfactorreceptorisrequiredforChlamydiatrachomatisdevelopment.BMCMicrobiol14:277.doi: 10.1186/s12866-014-0277-4 CrossRefGoogle Scholar
  109. PerryLL,FeilzerK,CaldwellHD(1997)ImmunitytoChlamydiatrachomatisismediatedbyThelper1cellsthroughIFN-gamma-dependentand-independentpathways.JImmunol158(7):3344–3352Google Scholar
  110. PetrilliV,PapinS,DostertC,MayorA,MartinonF,TschoppJ(2007)ActivationoftheNALP3inflammasomeistriggeredbylowintracellularpotassiumconcentration.CellDeathDiffer14(9):1583–1589.doi: 10.1038/sj.cdd.4402195 CrossRefGoogle Scholar
  111. PhillipsCampbellR,KintnerJ,WhittimoreJ,SchoborgRV(2012)Chlamydiamuridarumentersaviablebutnon-infectiousstateinamoxicillin-treatedBALB/cmice.MicrobesInfect14(13):1177–1185.doi: 10.1016/j.micinf.2012.07.017 CrossRefGoogle Scholar
  112. PillaDM,HagarJA,HaldarAK,MasonAK,DegrandiD,PfefferK,ErnstRK,YamamotoM,MiaoEA,CoersJ(2014)Guanylatebindingproteinspromotecaspase-11-dependentpyroptosisinresponsetocytoplasmicLPS.ProcNatlAcadSciUSA111(16):6046–6051.doi: 10.1073/pnas.1321700111 CrossRefGoogle Scholar
  113. PlataniasLC(2005)Mechanismsoftype-I-andtype-II-interferon-mediatedsignalling.NatRevImmunol5(5):375–386.doi: 10.1038/nri1604 CrossRefGoogle Scholar
  114. PrakashH,BeckerD,BohmeL,AlbertL,WitzenrathM,RosseauS,MeyerTF,RudelT(2009)cIAP-1controlsinnateimmunitytoC.pneumoniaepulmonaryinfection.PLoSONE4(8):e6519.doi: 10.1371/journal.pone.0006519 CrossRefGoogle Scholar
  115. PrebeckS,KirschningC,DurrS,daCostaC,DonathB,BrandK,RedeckeV,WagnerH,MiethkeT(2001)Predominantroleoftoll-likereceptor2versus4inChlamydiapneumoniae-inducedactivationofdendriticcells.JImmunol167(6):3316–3323Google Scholar
  116. PrustyBK,BohmeL,BergmannB,SieglC,KrauseE,MehlitzA,RudelT(2012)Imbalancedoxidativestresscauseschlamydialpersistenceduringnon-productivehumanherpesvirusco-infection.PLoSONE7(10):e47427.doi: 10.1371/journal.pone.0047427 CrossRefGoogle Scholar
  117. PrustyBK,KrohneG,RudelT(2013)Reactivationofchromosomallyintegratedhumanherpesvirus-6bytelomericcircleformation.PLoSGenet9(12):e1004033.doi: 10.1371/journal.pgen.1004033 CrossRefGoogle Scholar
  118. RajalingamK,SharmaM,PalandN,HurwitzR,ThieckO,OswaldM,MachuyN,RudelT(2006)IAP-IAPcomplexesrequiredforapoptosisresistanceofC.trachomatis-infectedcells.PLoSPathog2(10):e114.doi: 10.1371/journal.ppat.0020114 CrossRefGoogle Scholar
  119. RajalingamK,SharmaM,LohmannC,OswaldM,ThieckO,FroelichCJ,RudelT(2008)Mcl-1isakeyregulatorofapoptosisresistanceinChlamydiatrachomatis-infectedcells.PLoSONE3(9):e3102.doi: 10.1371/journal.pone.0003102 CrossRefGoogle Scholar
  120. RandowF,YouleRJ(2014)Selfandnonself:howautophagytargetsmitochondriaandbacteria.CellHostMicrobe15(4):403–411.doi: 10.1016/j.chom.2014.03.012 CrossRefGoogle Scholar
  121. RasmussenSJ,EckmannL,QuayleAJ,ShenL,ZhangYX,AndersonDJ,FiererJ,StephensRS,KagnoffMF(1997)SecretionofproinflammatorycytokinesbyepithelialcellsinresponsetoChlamydiainfectionsuggestsacentralroleforepithelialcellsinchlamydialpathogenesis.JClinInvest99(1):77–87.doi: 10.1172/JCI119136 CrossRefGoogle Scholar
  122. ReadTD,BrunhamRC,ShenC,GillSR,HeidelbergJF,WhiteO,HickeyEK,PetersonJ,UtterbackT,BerryK,BassS,LinherK,WeidmanJ,KhouriH,CravenB,BowmanC,DodsonR,GwinnM,NelsonW,DeBoyR,KolonayJ,McClartyG,SalzbergSL,EisenJ,FraserCM(2000)GenomesequencesofChlamydiatrachomatisMoPnandChlamydiapneumoniaeAR39.NucleicAcidsRes28(6):1397–1406Google Scholar
  123. RodelJ,GrosseC,YuH,WolfK,OttoGP,Liebler-TenorioE,Forsbach-BirkV,StraubeE(2012)PersistentChlamydiatrachomatisinfectionofHeLacellsmediatesapoptosisresistancethroughaChlamydiaprotease-likeactivityfactor-independentmechanismandinduceshighmobilitygroupbox1release.InfectImmun80(1):195–205.doi: 10.1128/IAI.05619-11 CrossRefGoogle Scholar
  124. RoshickC,WoodH,CaldwellHD,McClartyG(2006)Comparisonofgammainterferon-mediatedantichlamydialdefensemechanismsinhumanandmousecells.InfectImmun74(1):225–238.doi: 10.1128/IAI.74.1.225-238.2006 CrossRefGoogle Scholar
  125. RottenbergME,Gigliotti-RothfuchsA,WigzellH(2002)TheroleofIFN-gammaintheoutcomeofchlamydialinfection.CurrOpinImmunol14(4):444–451Google Scholar
  126. RudelT,KeppO,Kozjak-PavlovicV(2010)Interactionsbetweenbacterialpathogensandmitochondrialcelldeathpathways.NatRevMicrobiol8(10):693–705.doi: 10.1038/nrmicro2421 CrossRefGoogle Scholar
  127. RuppJ,GieffersJ,KlingerM,vanZandbergenG,WraseR,MaassM,SolbachW,DeiwickJ,Hellwig-BurgelT(2007)ChlamydiapneumoniaedirectlyinterfereswithHIF-1alphastabilizationinhumanhostcells.CellMicrobiol9(9):2181–2191.doi: 10.1111/j.1462-5822.2007.00948.x CrossRefGoogle Scholar
  128. SadlerAJ,WilliamsBR(2008)Interferon-inducibleantiviraleffectors.NatRevImmunol8(7):559–568.doi: 10.1038/nri2314 CrossRefGoogle Scholar
  129. Said-SadierN,PadillaE,LangsleyG,OjciusDM(2010)AspergillusfumigatusstimulatestheNLRP3inflammasomethroughapathwayrequiringROSproductionandtheSyktyrosinekinase.PLoSONE5(4):e10008.doi: 10.1371/journal.pone.0010008 CrossRefGoogle Scholar
  130. SanjuanMA,DillonCP,TaitSW,MoshiachS,DorseyF,ConnellS,KomatsuM,TanakaK,ClevelandJL,WithoffS,GreenDR(2007)Toll-likereceptorsignallinginmacrophageslinkstheautophagypathwaytophagocytosis.Nature450(7173):1253–1257.doi: 10.1038/nature06421 CrossRefGoogle Scholar
  131. SanjuanMA,MilastaS,GreenDR(2009)Toll-likereceptorsignalinginthelysosomalpathways.ImmunolRev227(1):203–220.doi: 10.1111/j.1600-065X.2008.00732.x CrossRefGoogle Scholar
  132. SchneiderWM,ChevillotteMD,RiceCM(2014)Interferon-stimulatedgenes:acomplexwebofhostdefenses.AnnuRevImmunol32:513–545.doi: 10.1146/annurev-immunol-032713-120231 CrossRefGoogle Scholar
  133. SchroderK,TschoppJ(2010)Theinflammasomes.Cell140(6):821–832.doi: 10.1016/j.cell.2010.01.040 CrossRefGoogle Scholar
  134. ScidmoreMA,HackstadtT(2001)Mammalian14-3-3betaassociateswiththeChlamydiatrachomatisinclusionmembraneviaitsinteractionwithIncG.MolMicrobiol39(6):1638–1650Google Scholar
  135. Shamas-DinA,KaleJ,LeberB,AndrewsDW(2013)MechanismsofactionofBcl-2familyproteins.ColdSpringHarbPerspectBiol5(4):a008714.doi: 10.1101/cshperspect.a008714 CrossRefGoogle Scholar
  136. ShaoW,YeretssianG,DoironK,HussainSN,SalehM(2007)Thecaspase-1digestomeidentifiestheglycolysispathwayasatargetduringinfectionandsepticshock.JBiolChem282(50):36321–36329.doi: 10.1074/jbc.M708182200 CrossRefGoogle Scholar
  137. SharmaM,RudelT(2009)ApoptosisresistanceinChlamydia-infectedcells:afateworsethandeath?FEMSImmunolMedMicrobiol55(2):154–161.doi: 10.1111/j.1574-695X.2008.00515.x CrossRefGoogle Scholar
  138. SharmaM,MachuyN,BohmeL,KarunakaranK,MaurerAP,MeyerTF,RudelT(2011)HIF-1alphaisinvolvedinmediatingapoptosisresistancetoChlamydiatrachomatis-infectedcells.CellMicrobiol13(10):1573–1585.doi: 10.1111/j.1462-5822.2011.01642.x CrossRefGoogle Scholar
  139. ShenoyAR,WellingtonDA,KumarP,KassaH,BoothCJ,CresswellP,MacMickingJD(2012)GBP5promotesNLRP3inflammasomeassemblyandimmunityinmammals.Science336(6080):481–485.doi: 10.1126/science.1217141 CrossRefGoogle Scholar
  140. ShimadaK,CrotherTR,KarlinJ,ChenS,ChibaN,RamanujanVK,VergnesL,OjciusDM,ArditiM(2011)Caspase-1dependentIL-1betasecretioniscriticalforhostdefenseinamousemodelofChlamydiapneumoniaelunginfection.PLoSONE6(6):e21477.doi: 10.1371/journal.pone.0021477 CrossRefGoogle Scholar
  141. ShimadaK,CrotherTR,ArditiM(2012)InnateimmuneresponsestoChlamydiapneumoniaeinfection:roleofTLRs,NLRs,andtheinflammasome.MicrobesInfect14(14):1301–1307.doi: 10.1016/j.micinf.2012.08.004 CrossRefGoogle Scholar
  142. ShinS,BrodskyIE(2015)Theinflammasome:Learningfrombacterialevasionstrategies.SeminImmunol27(2):102–110.doi: 10.1016/j.smim.2015.03.006 CrossRefGoogle Scholar
  143. SieglC,RudelT(2015)Modulationofp53duringbacterialinfections.NatRevMicrobiol13(12):741–748.doi: 10.1038/nrmicro3537 CrossRefGoogle Scholar
  144. SieglC,PrustyBK,KarunakaranK,WischhusenJ,RudelT(2014)Tumorsuppressorp53altershostcellmetabolismtolimitChlamydiatrachomatisinfection.CellRep9(3):918–929.doi: 10.1016/j.celrep.2014.10.004 CrossRefGoogle Scholar
  145. SimonS,HilbiH(2015)Subversionofcell-autonomousimmunityandcellmigrationbyLegionellapneumophilaeffectors.FrontImmunol6:447.doi: 10.3389/fimmu.2015.00447 CrossRefGoogle Scholar
  146. StrattonCW,SriramS(2003)AssociationofChlamydiapneumoniaewithcentralnervoussystemdisease.MicrobesInfect5(13):1249–1253Google Scholar
  147. SuH,McClartyG,DongF,HatchGM,PanZK,ZhongG(2004)ActivationofRaf/MEK/ERK/cPLA2signalingpathwayisessentialforchlamydialacquisitionofhostglycerophospholipids.JBiolChem279(10):9409–9416.doi: 10.1074/jbc.M312008200 CrossRefGoogle Scholar
  148. SubbarayalP,KarunakaranK,WinklerAC,RotherM,GonzalezE,MeyerTF,RudelT(2015)EphrinA2receptor(EphA2)isaninvasionandintracellularsignalingreceptorforChlamydiatrachomatis.PLoSPathog11(4):e1004846.doi: 10.1371/journal.ppat.1004846 CrossRefGoogle Scholar
  149. SunHS,EngEW,JeganathanS,SinAT,PatelPC,GraceyE,InmanRD,TerebiznikMR,HarrisonRE(2012)Chlamydiatrachomatisvacuolematurationininfectedmacrophages.JLeukocBiol92(4):815–827.doi: 10.1189/jlb.0711336 CrossRefGoogle Scholar
  150. TakeuchiO,AkiraS(2010)Patternrecognitionreceptorsandinflammation.Cell140(6):805–820.doi: 10.1016/j.cell.2010.01.022 CrossRefGoogle Scholar
  151. ThomasLW,LamC,EdwardsSW(2010)Mcl-1;themolecularregulationofproteinfunction.FEBSLett584(14):2981–2989.doi: 10.1016/j.febslet.2010.05.061 CrossRefGoogle Scholar
  152. ThorpeLM,YuzugulluH,ZhaoJJ(2015)PI3Kincancer:divergentrolesofisoforms,modesofactivationandtherapeutictargeting.NatRevCancer15(1):7–24.doi: 10.1038/nrc3860 CrossRefGoogle Scholar
  153. vanWijkSJ,FiskinE,PutyrskiM,PampaloniF,HouJ,WildP,KenscheT,GreccoHE,BastiaensP,DikicI(2012)Fluorescence-basedsensorstomonitorlocalizationandfunctionsoflinearandK63-linkedubiquitinchainsincells.MolCell47(5):797–809.doi: 10.1016/j.molcel.2012.06.017 CrossRefGoogle Scholar
  154. VerbekeP,Welter-StahlL,YingS,HansenJ,HackerG,DarvilleT,OjciusDM(2006)RecruitmentofBADbytheChlamydiatrachomatisvacuolecorrelateswithhost-cellsurvival.PLoSPathog2(5):e45.doi: 10.1371/journal.ppat.0020045 CrossRefGoogle Scholar
  155. VergneI,ChuaJ,SinghSB,DereticV(2004)Cellbiologyofmycobacteriumtuberculosisphagosome.AnnuRevCellDevBiol20:367–394.doi: 10.1146/annurev.cellbio.20.010403.114015 CrossRefGoogle Scholar
  156. WrightHR,TurnerA,TaylorHR(2008)Trachoma.Lancet371(9628):1945–1954.doi: 10.1016/S0140-6736(08)60836-3 CrossRefGoogle Scholar
  157. YangSC,HungCF,AljuffaliIA,FangJY(2015)TherolesofthevirulencefactorIpaBinShigellaspp.intheescapefromimmunecellsandinvasionofepithelialcells.MicrobiolRes181:43–51.doi: 10.1016/j.micres.2015.08.006 CrossRefGoogle Scholar
  158. YingS,FischerSF,PettengillM,ConteD,PaschenSA,OjciusDM,HackerG(2006)CharacterizationofhostcelldeathinducedbyChlamydiatrachomatis.InfectImmun74(11):6057–6066.doi: 10.1128/IAI.00760-06 CrossRefGoogle Scholar
  159. YingS,ChristianJG,PaschenSA,HackerG(2008)ChlamydiatrachomatiscanprotecthostcellsagainstapoptosisintheabsenceofcellularInhibitorofApoptosisProteinsandMcl-1.MicrobesInfect10(1):97–101.doi: 10.1016/j.micinf.2007.10.005 CrossRefGoogle Scholar
  160. ZhaoY,YangJ,ShiJ,GongYN,LuQ,XuH,LiuL,ShaoF(2011)TheNLRC4inflammasomereceptorsforbacterialflagellinandtypeIIIsecretionapparatus.Nature477(7366):596–600.doi: 10.1038/nature10510 CrossRefGoogle Scholar
  161. ZhouR,YazdiAS,MenuP,TschoppJ(2011)AroleformitochondriainNLRP3inflammasomeactivation.Nature469(7329):221–225.doi: 10.1038/nature09663 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Open Access This chapter is distributed under the terms of the Creative Commons Attribution Noncommercial License, which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Authors and Affiliations

  1. 1.Department of Microbiology and BiocenterUniversity of WürzburgWuerzburgGermany

Personalised recommendations