Differential modulation of TNF-α-induced apoptosis by Neisseria meningitidis

PLoS Pathogens

Volumn 5, Issue 5, 2009, Pages

  Deghmane, Ala Eddine ^a   Veckerlé, Carole ^a,b   Giorgini, Dario ^a   Hong, Eva ^a   Ruckly, Corinne ^a   Taha, Muhamed Kheir ^a  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; DNA; ENDOTOXIN; FLUORESCEIN ISOTHIOCYANATE; LIPOCORTIN 5; LIPOOLIGOSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR 1; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR 1;

APOPTOSIS; ARTICLE; BACTERIUM ISOLATE; CELL PROTECTION; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DNA FRAGMENTATION; ECOLOGICAL NICHE; ENZYME ASSAY; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; INFLAMMATION; MODULATION; NASOPHARYNX; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; STAINING; ANALYSIS OF VARIANCE; CELL ADHESION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; HETEROZYGOTE; MENINGOCOCCOSIS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS;

ANALYSIS OF VARIANCE; APOPTOSIS; BACTERIAL PROTEINS; CARRIER STATE; CELL ADHESION; CELL LINE, TUMOR; ENDOTOXINS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MENINGOCOCCAL INFECTIONS; MICROSCOPY, FLUORESCENCE; NEISSERIA MENINGITIDIS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 67249114315     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000405     Document Type: Article

References (69)

1. van Deuren M, Brandtzaeg P, van der Meer JW (2000) Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13: 144-166, table of contents. (Pubitemid 30039347)
2. Klein NJ, Ison CA, Peakman M, Levin M, Hammerschmidt S, et al. (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. (Pubitemid 26006817)
3. Virji M, Kayhty H, Ferguson DJ, Alexandrescu C, Heckels JE, et al. (1991) The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells. Mol Microbiol 5: 1831-1841. (Pubitemid 21896215)
4. Mercier JC, Beaufils F, Hartmann JF, Azema D (1988) Hemodynamic patterns of meningococcal shock in children. Crit Care Med 16: 27-33. (Pubitemid 18117859)
5. Virji M, Makepeace K, Ferguson DJ, Achtman M, Moxon ER (1993) Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10: 499-510. (Pubitemid 23334431)
6. Virji M, Makepeace K, Ferguson DJ, Achtman M, Sarkari J, et al. (1992) Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol 6: 2785-2795.
7. Birkness KA, Swisher BL, White EH, Long EG, Ewing EP Jr, et al. (1995) A tissue culture bilayer model to study the passage of Neisseria meningitidis. Infect Immun 63: 402-409.
8. Stephens DS, Farley MM (1991) Pathogenic events during infection of the human nasopharynx with Neisseria meningitidis and Haemophilus influenzae. Rev Infect Dis 13: 22-33.
9. Warren HS Jr, Gonzalez RG, Tian D (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.
10. Gao LY, Kwaik YA (2000) The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol 8: 306-313. (Pubitemid 30421064)
11. DeLeo FR (2004) Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis 9: 399-413. (Pubitemid 38987576)
12. Grassme H, Jendrossek V, Gulbins E (2001) Molecular mechanisms of bacteria induced apoptosis. Apoptosis 6: 441-445. (Pubitemid 33078754)
13. Weinrauch Y, Zychlinsky A (1999) The induction of apoptosis by bacterial pathogens. Annu Rev Microbiol 53: 155-187. (Pubitemid 29503729)
14. Guzman CA, Domann E, Rohde M, Bruder D, Darji A, et al. (1996) Apoptosis of mouse dendritic cells is triggered by listeriolysin, the major virulence determinant of Listeria monocytogenes. Mol Microbiol 20: 119-126. (Pubitemid 26126050)
15. Schubert-Unkmeir A, Sokolova O, Panzner U, Eigenthaler M, Frosch M (2007) Gene expression pattern in human brain endothelial cells in response to Neisseria meningitidis. Infect Immun 75: 899-914. (Pubitemid 46203455)
16. Muller A, Gunther D, Dux F, Naumann M, Meyer TF, et al. (1999) Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. Embo J 18: 339-352. (Pubitemid 29041943)
17. Muller A, Gunther D, Brinkmann V, Hurwitz R, Meyer TF, et al. (2000) Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. Embo J 19: 5332-5343. (Pubitemid 30795907)
18. Morales P, Reyes P, Vargas M, Rios M, Imarai M, et al. (2006) Infection of human fallopian tube epithelial cells with Neisseria gonorrhoeae protects cells from tumor necrosis factor alpha-induced apoptosis. Infect Immun 74: 3643-3650. (Pubitemid 43794555)
19. Maisey K, Nardocci G, Imarai M, Cardenas H, Rios M, et al. (2003) Expression of proinflammatory cytokines and receptors by human fallopian tubes in organ culture following challenge with Neisseria gonorrhoeae. Infect Immun 71: 527-532. (Pubitemid 36026059)
20. Massari P, Ho Y, Wetzler LM (2000) Neisseria meningitidis porin PorB interacts with mitochondria and protects cells from apoptosis. Proc Natl Acad Sci U S A 97: 9070-9075. (Pubitemid 30626675)
21. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, et al. (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. (Pubitemid 28135868)
22. Yazdankhah SP, Kriz P, Tzanakaki G, Kremastinou J, Kalmusova J, et al. (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. (Pubitemid 39506223)
23. Jolley KA, Kalmusova J, Feil EJ, Gupta S, Musilek M, et al. (2000) Carried meningococci in the Czech Republic: a diverse recombining population. J Clin Microbiol 38: 4492-4498. (Pubitemid 32244539)
24. Claus H, Maiden MC, Wilson DJ, McCarthy ND, Jolley KA, et al. (2005) Genetic analysis of meningococci carried by children and young adults. J Infect Dis 191: 1263-1271. (Pubitemid 40503654)
25. Zarantonelli ML, Lancellotti M, Deghmane AE, Giorgini D, Hong E, et al. (2008) Hyperinvasive genotypes of Neisseria meningitidis in France. Clin Microbiol Infect 14: 467-472.
26. Zughaier SM, Zimmer SM, Datta A, Carlson RW, Stephens DS (2005) Differential induction of the toll-like receptor 4-MyD88-dependent and -independent signaling pathways by endotoxins. Infect Immun 73: 2940-2950. (Pubitemid 40575735)
27. Golstein P, Ojcius DM, Young JD (1991) Cell death mechanisms and the immune system. Immunol Rev 121: 29-65.
28. Vandenabeele P, Declercq W, Beyaert R, Fiers W (1995) Two tumour necrosis factor receptors: structure and function. Trends Cell Biol 5: 392-399.
29. Engelmann H, Novick D, Wallach D (1990) Two tumor necrosis factor-binding proteins purified from human urine. Evidence for immunological cross-reactivity with cell surface tumor necrosis factor receptors. J Biol Chem 265: 1531-1536. (Pubitemid 20048977)
30. Nophar Y, Kemper O, Brakebusch C, Englemann H, Zwang R, et al. (1990) Soluble forms of tumor necrosis factor receptors (TNF-Rs). The cDNA for the type I TNF-R, cloned using amino acid sequence data of its soluble form, encodes both the cell surface and a soluble form of the receptor. Embo J 9: 3269-3278.
31. Novick D, Engelmann H, Wallach D, Rubinstein M (1989) Soluble cytokine receptors are present in normal human urine. J Exp Med 170: 1409-1414. (Pubitemid 19250702)
32. Brandtzaeg P, Bjerre A, Ovstebo R, Brusletto B, Joo GB, et al. (2001) Neisseria meningitidis lipopolysaccharides in human pathology. J Endotoxin Res 7: 401-420. (Pubitemid 34051307)
33. Taha MK (2000) Neisseria meningitidis induces the expression of the TNF-alpha gene in endothelial cells. Cytokine 12: 21-25. (Pubitemid 30042677)
34. Stephens DS, Greenwood B, Brandtzaeg P (2007) Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369: 2196-2210. (Pubitemid 46977462)
35. Emonts M, Hazelzet JA, de Groot R, Hermans PW (2003) Host genetic determinants of Neisseria meningitidis infections. Lancet Infect Dis 3: 565-577. (Pubitemid 37064536)
36. Taha MK, Alonso JM (2008) Molecular epidemiology of infectious diseases: the example of meningococcal disease. Res Microbiol 159: 62-66.
37. Schoen C, Blom J, Claus H, Schramm-Gluck A, Brandt P, et al. (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. (Pubitemid 351723577)
38. Zarantonelli ML, Carlier JP, Alonso JM, Taha MK (2003) Insertional inactivation of the lpxA gene involved in the biosynthesis of lipid A in Neisseria meningitidis resulted in lpxA/lpxA::aph-3′ heterodiploids. FEMS Microbiol Lett 226: 51-56. (Pubitemid 38444896)
39. Naumann M, Rudel T, Meyer TF (1999) Host cell interactions and signalling with Neisseria gonorrhoeae. Curr Opin Microbiol 2: 62-70. (Pubitemid 29130217)
40. Jendrossek V, Fillon S, Belka C, Muller I, Puttkammer B, et al. (2003) Apoptotic response of Chang cells to infection with Pseudomonas aeruginosa strains PAK and PAO-I: molecular ordering of the apoptosis signaling cascade and role of type IV pili. Infect Immun 71: 2665-2673. (Pubitemid 36519882)
41. Abul-Milh M, Wu Y, Lau B, Lingwood CA, Barnett Foster D (2001) Induction of epithelial cell death including apoptosis by enteropathogenic Escherichia coli expressing bundle-forming pili. Infect Immun 69: 7356-7364. (Pubitemid 33086559)
42. MacRedmond R, Greene C, Taggart CC, McElvaney N, O'Neill S (2005) Respiratory epithelial cells require Toll-like receptor 4 for induction of human beta-defensin 2 by lipopolysaccharide. Respir Res 6: 116. (Pubitemid 41554936)
43. Narayanan K, Seufzer BJ, Brockman-Schneider RA, Gern JE, Balakrishnan A, et al. (2002) CD14-dependent activation of NF-kappaB by filarial parasitic sheath proteins. Cell Biol Int 26: 43-54. (Pubitemid 34174406)
44. O'Neill LA (2006) How Toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 18: 3-9. (Pubitemid 43049641)
45. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088. (Pubitemid 29001265)
46. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, et al. (1999) Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11: 443-451. (Pubitemid 29504199)
47. Singleton TE, Massari P, Wetzler LM (2005) Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J Immunol 174: 3545-3550. (Pubitemid 40354063)
48. Massari P, Visintin A, Gunawardana J, Halmen KA, King CA, et al. (2006) Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J Immunol 176: 2373-2380. (Pubitemid 43201686)
49. Campagnari AA, Wild LM, Griffiths GE, Karalus RJ, Wirth MA, et al. (1991) Role of lipooligosaccharides in experimental dermal lesions caused by Haemophilus ducreyi. Infect Immun 59: 2601-2608.
50. Galanos C, Freudenberg MA (1993) Mechanisms of endotoxin shock and endotoxin hypersensitivity. Immunobiology 187: 346-356. (Pubitemid 23150777)
51. Quagliarello V, Scheld WM (1992) Bacterial meningitis: pathogenesis, pathophysiology, and progress. N Engl J Med 327: 864-872.
52. Sprong T, van der Ley P, Steeghs L, Taw WJ, Verver-Janssen TJ, et al. (2002) Neisseria meningitidis can induce pro-inflammatory cytokine production via pathways independent from CD14 and toll-like receptor 4. Eur Cytokine Netw 13: 411-417. (Pubitemid 36174098)
53. Zughaier SM, Tzeng YL, Zimmer SM, Datta A, Carlson RW, et al. (2004) Neisseria meningitidis lipooligosaccharide structure-dependent activation of the macrophage CD14/Toll-like receptor 4 pathway. Infect Immun 72: 371-380. (Pubitemid 38018198)
54. Perfettini JL, Darville T, Gachelin G, Souque P, Huerre M, et al. (2000) Effect of Chlamydia trachomatis infection and subsequent tumor necrosis factor alpha secretion on apoptosis in the murine genital tract. Infect Immun 68: 2237-2244. (Pubitemid 30164860)
55. Lindberg K, Rynnel-Dagoo B, Sundqvist KG (1994) Cytokines in nasopharyngeal secretions; evidence for defective IL-1 beta production in children with recurrent episodes of acute otitis media. Clin Exp Immunol 97: 396-402. (Pubitemid 24283881)
56. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104: 487-501. (Pubitemid 32201945)
57. McGee ZA, Jensen RL, Clemens CM, Taylor-Robinson D, Johnson AP, et al. (1999) Gonococcal infection of human fallopian tube mucosa in organ culture: relationship of mucosal tissue TNF-alpha concentration to sloughing of ciliated cells. Sex Transm Dis 26: 160-165. (Pubitemid 29122740)
58. Stephens DS, Zimmer SM (2002) Pathogenesis, Therapy, and Prevention of Meningococcal Sepsis. Curr Infect Dis Rep 4: 377-386.
59. Moss ML, Jin SL, Becherer JD, Bickett DM, Burkhart W, et al. (1997) Structural features and biochemical properties of TNF-alpha converting enzyme (TACE). J Neuroimmunol 72: 127-129. (Pubitemid 27062767)
60. Paland N, Bohme L, Gurumurthy RK, Maurer A, Szczepek AJ, et al. (2008) Reduced display of tumor necrosis factor receptor I at the host cell surface supports infection with Chlamydia trachomatis. J Biol Chem 283: 6438-6448.
61. Gomez MI, Seaghdha MO, Prince AS (2007) Staphylococcus aureus protein A activates TACE through EGFR-dependent signaling. Embo J 26: 701-709. (Pubitemid 46253855)
62. Gomez MI, O'Seaghdha M, Magargee M, Foster TJ, Prince AS (2006) Staphylococcus aureus protein A activates TNFR1 signaling through conserved IgG binding domains. J Biol Chem 281: 20190-20196. (Pubitemid 44065793)
63. Gomez MI, Sokol SH, Muir AB, Soong G, Bastien J, et al. (2005) Bacterial induction of TNF-alpha converting enzyme expression and IL-6 receptor alpha shedding regulates airway inflammatory signaling. J Immunol 175: 1930-1936. (Pubitemid 41023100)
64. Kellogg DS Jr, Peacock WL Jr, Deacon WE, Brown L, Pirkle DI (1963) Neisseria Gonorrhoeae. I. Virulence Genetically Linked to Clonal Variation. J Bacteriol 85: 1274-1279.
65. Taha MK, Morand PC, Pereira Y, Eugene E, Giorgini D, et al. (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. (Pubitemid 28293539)
66. Deghmane AE, Giorgini D, Larribe M, Alonso JM, Taha MK (2002) Downregulation of pili and capsule of Neisseria meningitidis upon contact with epithelial cells is mediated by CrgA regulatory protein. Mol Microbiol 43: 1555-1564. (Pubitemid 34595546)
67. Sciavolino PJ, Lee TH, Vilcek J (1992) Overexpression of metallothionein confers resistance to the cytotoxic effect of TNF with cadmium in MCF-7 breast carcinoma cells. Lymphokine Cytokine Res 11: 265-270.
68. Sendide K, Reiner NE, Lee JS, Bourgoin S, Talal A, et al. (2005) Cross-talk between CD14 and complement receptor 3 promotes phagocytosis of mycobacteria: regulation by phosphatidylinositol 3-kinase and cytohesin-1. J Immunol 174: 4210-4219. (Pubitemid 40396001)
69. Bonnah RA, Hoelter J, Steeghs L, Enns CA, So M, et al. (2005) Lipooligosaccharide-independent alteration of cellular homeostasis in Neisseria meningitidis-infected epithelial cells. Cell Microbiol 7: 869-885. (Pubitemid 40740381)