Late Repression of NF-κB Activity by Invasive but Not Non-Invasive Meningococcal Isolates Is Required to Display Apoptosis of Epithelial Cells

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Meningococcal invasive isolates of the ST-11 clonal complex are most frequently associated with disease and rarely found in carriers. Unlike carriage isolates, invasive isolates induce apoptosis in epithelial cells through the TNF-α signaling pathway. While invasive and non-invasive isolates are both able to trigger the TLR4/MyD88 pathway in lipooligosaccharide (LOS)-dependant manner, we show that only non-invasive isolates were able to induce sustained NF-κB activity in infected epithelial cells. ST-11 invasive isolates initially triggered a strong NF-κB activity in infected epithelial cells that was abolished after 9h of infection and was associated with sustained activation of JNK, increased levels of membrane TNFR1, and induction of apoptosis. In contrast, infection with carriage isolates lead to prolonged activation of NF-κB that was associated with a transient activation of JNK increased TACE/ADAM17-mediated shedding of TNFR1 and protection against apoptosis. Our data provide insights to understand the meningococcal duality between invasiveness and asymptomatic carriage.

Vyšlo v časopise: Late Repression of NF-κB Activity by Invasive but Not Non-Invasive Meningococcal Isolates Is Required to Display Apoptosis of Epithelial Cells. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002403
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002403

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1. PeltolaH 1983 Meningococcal disease: still with us. Rev Infect Dis 5 71 91

2. SchuchatARobinsonKWengerJDHarrisonLHFarleyM 1997 Bacterial meningitis in the United States in 1995. Active Surveillance Team. N Engl J Med 337 970 976

3. van DeurenMBrandtzaegPvan der MeerJW 2000 Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13 144 166 table of contents

4. CartwrightKAStuartJMJonesDMNoahND 1987 The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol Infect 99 591 601

5. OrrHJGraySJMacdonaldMStuartJM 2003 Saliva and meningococcal transmission. Emerg Infect Dis 9 1314 1315

6. GoldschneiderIGotschlichECArtensteinMS 1969 Human immunity to the meningococcus. II. Development of natural immunity. J Exp Med 129 1327 1348

7. DensenP 1989 Interaction of complement with Neisseria meningitidis and Neisseria gonorrhoeae. Clin Microbiol Rev 2 Suppl S11 17

8. EmontsMHazelzetJAde GrootRHermansPW 2003 Host genetic determinants of Neisseria meningitidis infections. Lancet Infect Dis 3 565 577

9. MaidenMCBygravesJAFeilEMorelliGRussellJE 1998 Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95 3140 3145

10. CaugantDA 1998 Population genetics and molecular epidemiology of Neisseria meningitidis. Apmis 106 505 525

11. YazdankhahSPKrizPTzanakakiGKremastinouJKalmusovaJ 2004 Distribution of serogroups and genotypes among disease-associated and carried isolates of Neisseria meningitidis from the Czech Republic, Greece, and Norway. J Clin Microbiol 42 5146 5153

12. JolleyKAKalmusovaJFeilEJGuptaSMusilekM 2000 Carried meningococci in the Czech Republic: a diverse recombining population. J Clin Microbiol 38 4492 4498

13. ZarantonelliMLLancellottiMDeghmaneAEGiorginiDHongE 2008 Hyperinvasive genotypes of Neisseria meningitidis in France. Clin Microbiol Infect 14 467 472

14. SchoenCBlomJClausHSchramm-GluckABrandtP 2008 Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc Natl Acad Sci U S A 105 3473 3478

15. KleinNJIsonCAPeakmanMLevinMHammerschmidtS 1996 The influence of capsulation and lipooligosaccharide structure on neutrophil adhesion molecule expression and endothelial injury by Neisseria meningitidis. J Infect Dis 173 172 179

16. VirjiMKayhtyHFergusonDJAlexandrescuCHeckelsJE 1991 The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5 1831 1841

17. MercierJCBeaufilsFHartmannJFAzemaD 1988 Hemodynamic patterns of meningococcal shock in children. Crit Care Med 16 27 33

18. BirknessKASwisherBLWhiteEHLongEGEwingEPJr 1995 A tissue culture bilayer model to study the passage of Neisseria meningitidis. Infect Immun 63 402 409

19. StephensDSFarleyMM 1991 Pathogenic events during infection of the human nasopharynx with Neisseria meningitidis and Haemophilus influenzae. Rev Infect Dis 13 22 33

20. ReadRCFoxAMillerKGrayTJonesN 1995 Experimental infection of human nasal mucosal explants with Neisseria meningitidis. J Med Microbiol 42 353 361

21. WarrenHSJrGonzalezRGTianD 2003 Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 38-2003. A 12-year-old girl with fever and coma. N Engl J Med 349 2341 2349

22. DeghmaneAEVeckerleCGiorginiDHongERucklyC 2009 Differential modulation of TNF-alpha-induced apoptosis by Neisseria meningitidis. PLoS Pathog 5 e1000405

23. BarnesPJKarinM 1997 Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 336 1066 1071

24. RothwarfDMKarinM The NF-kappa B activation pathway: a paradigm in information transfer from membrane to nucleus. Sci STKE 1999: RE1

25. WangCYMayoMWKornelukRGGoeddelDVBaldwinASJr 1998 NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281 1680 1683

26. RhenMErikssonSPetterssonS 2000 Bacterial adaptation to host innate immunity responses. Curr Opin Microbiol 3 60 64

27. KawaiTAkiraS 2006 TLR signaling. Cell Death Differ 13 816 825

28. MedzhitovRPreston-HurlburtPKoppEStadlenAChenC 1998 MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 2 253 258

29. YamamotoMSatoSMoriKHoshinoKTakeuchiO 2002 Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 169 6668 6672

30. YamamotoMSatoSHemmiHSanjoHUematsuS 2002 Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420 324 329

31. AderemAUlevitchRJ 2000 Toll-like receptors in the induction of the innate immune response. Nature 406 782 787

32. JensenTJLooMAPindSWilliamsDBGoldbergAL 1995 Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83 129 135

33. RockKLGrammCRothsteinLClarkKSteinR 1994 Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78 761 771

34. BegAABaltimoreD 1996 An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274 782 784

35. LiuZGHsuHGoeddelDVKarinM 1996 Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87 565 576

36. Van AntwerpDJMartinSJKafriTGreenDRVermaIM 1996 Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274 787 789

37. WangCYMayoMWBaldwinASJr 1996 TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274 784 787

38. WuMLeeHBellasRESchauerSLArsuraM 1996 Inhibition of NF-kappaB/Rel induces apoptosis of murine B cells. Embo J 15 4682 4690

39. MercurioFZhuHMurrayBWShevchenkoABennettBL 1997 IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278 860 866

40. PalombellaVJRandoOJGoldbergALManiatisT 1994 The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78 773 785

41. BlackRARauchCTKozloskyCJPeschonJJSlackJL 1997 A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385 729 733

42. MossMLJinSLBechererJDBickettDMBurkhartW 1997 Structural features and biochemical properties of TNF-alpha converting enzyme (TACE). J Neuroimmunol 72 127 129

43. GalloisCHabibATaoJMoulinSMacloufJ 1998 Role of NF-kappaB in the antiproliferative effect of endothelin-1 and tumor necrosis factor-alpha in human hepatic stellate cells. Involvement of cyclooxygenase-2. J Biol Chem 273 23183 23190

44. JohnsonSEDormanCMBolanowskiSA 2002 Inhibition of myogenin expression by activated Raf is not responsible for the block to avian myogenesis. J Biol Chem 277 28742 28748

45. BennettBLSasakiDTMurrayBWO'LearyECSakataST 2001 SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 98 13681 13686

46. TangGMinemotoYDiblingBPurcellNHLiZ 2001 Inhibition of JNK activation through NF-kappaB target genes. Nature 414 313 317

47. De SmaeleEZazzeroniFPapaSNguyenDUJinR 2001 Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414 308 313

48. CoyneCBVanhookMKGamblingTMCarsonJLBoucherRC 2002 Regulation of airway tight junctions by proinflammatory cytokines. Mol Biol Cell 13 3218 3234

49. SchmitzHFrommMBentzelCJScholzPDetjenK 1999 Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J Cell Sci 112 (Pt 1) 137 146

50. GitterAHBendfeldtKSchulzkeJDFrommM 2000 Leaks in the epithelial barrier caused by spontaneous and TNF-alpha-induced single-cell apoptosis. Faseb J 14 1749 1753

51. MattilaPSCarlsonP 1998 Pharyngolaryngitis caused by Neisseria meningitidis. Scand J Infect Dis 30 198 200

52. HsuLCParkJMZhangKLuoJLMaedaS 2004 The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428 341 345

53. ZhangYBliskaJB 2003 Role of Toll-like receptor signaling in the apoptotic response of macrophages to Yersinia infection. Infect Immun 71 1513 1519

54. VogelSNFentonM 2003 Toll-like receptor 4 signalling: new perspectives on a complex signal-transduction problem. Biochem Soc Trans 31 664 668

55. TakedaKAkiraS 2004 TLR signaling pathways. Semin Immunol 16 3 9

56. FitzgeraldKARoweDCBarnesBJCaffreyDRVisintinA 2003 LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J Exp Med 198 1043 1055

57. ChoiKBWongFHarlanJMChaudharyPMHoodL 1998 Lipopolysaccharide mediates endothelial apoptosis by a FADD-dependent pathway. J Biol Chem 273 20185 20188

58. RuckdeschelKMannelOSchrottnerP 2002 Divergence of apoptosis-inducing and preventing signals in bacteria-faced macrophages through myeloid differentiation factor 88 and IL-1 receptor-associated kinase members. J Immunol 168 4601 4611

59. KlumppDJWeiserACSenguptaSForrestalSGBatlerRA 2001 Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-kappaB. Infect Immun 69 6689 6695

60. MonackDMMecsasJBouleyDFalkowS 1998 Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J Exp Med 188 2127 2137

61. SingletonTEMassariPWetzlerLM 2005 Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J Immunol 174 3545 3550

62. TakamuneYIkebeTNaganoOShinoharaM 2008 Involvement of NF-kappaB-mediated maturation of ADAM-17 in the invasion of oral squamous cell carcinoma. Biochem Biophys Res Commun 365 393 398

63. SokolovaOHeppelNJagerhuberRKimKSFroschM 2004 Interaction of Neisseria meningitidis with human brain microvascular endothelial cells: role of MAP- and tyrosine kinases in invasion and inflammatory cytokine release. Cell Microbiol 6 1153 1166

64. JohnsonGLLapadatR 2002 Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298 1911 1912

65. SzatanikMHongERucklyCLedroitMGiorginiD 2011 Experimental meningococcal sepsis in congenic transgenic mice expressing human transferrin. PLoS ONE 6 e22210

66. Guinea-ViniegraJZenzRScheuchHHniszDHolcmannM 2009 TNFalpha shedding and epidermal inflammation are controlled by Jun proteins. Genes Dev 23 2663 2674

67. DerbignyWAHongSCKerrMSTemkitMJohnsonRM 2007 Chlamydia muridarum infection elicits a beta interferon response in murine oviduct epithelial cells dependent on interferon regulatory factor 3 and TRIF. Infect Immun 75 1280 1290

68. HanahanD 1983 Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166 557 580

69. KelloggDSJrPeacockWLJrDeaconWEBrownLPirkleDI 1963 Neisseria Gonorrhoeae. I. Virulence Genetically Linked to Clonal Variation. J Bacteriol 85 1274 1279

70. DeghmaneAEGiorginiDLarribeMAlonsoJMTahaMK 2002 Down-regulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol Microbiol 43 1555 1564

71. TahaMKMorandPCPereiraYEugeneEGiorginiD 1998 Pilus-mediated adhesion of Neisseria meningitidis: the essential role of cell contact-dependent transcriptional upregulation of the PilC1 protein. Mol Microbiol 28 1153 1163

72. JarvisGALiJSwansonKV 1999 Invasion of human mucosal epithelial cells by Neisseria gonorrhoeae upregulates expression of intercellular adhesion molecule 1 (ICAM-1). Infect Immun 67 1149 1156

73. PhilpottDJBelaidDTroubadourPThibergeJMTankovicJ 2002 Reduced activation of inflammatory responses in host cells by mouse-adapted Helicobacter pylory isolates. Cell Microbiol 4 285 296

74. Schmidt-UllrichRMemetSLilienbaumAFeuillardJRaphaelM 1996 NF-kappaB activity in transgenic mice: developmental regulation and tissue specificity. Development 122 2117 2128

75. DeghmaneAEPetitSTopilkoAPereiraYGiorginiD 2000 Intimate adhesion of Neisseria meningitidis to human epithelial cells is under the control of the crgA gene, a novel LysR-type transcriptional regulator. Embo J 19 1068 1078