EstA protein, a novel virulence factor of Streptococcus pneumoniae, induces nitric oxide and pro-inflammatory cytokine production in RAW 264.7 macrophages through NF-κB/MAPK

Microbial Pathogenesis

Volumn 47, Issue 4, 2009, Pages 196-201

  Kang, Eun Hee ^a   Gebru, Elias ^a   Kim, Myung Hee ^b   Cheng, Henrique ^c   Park, Seung Chun ^a  

^a Kyungpook National University   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ESTERASE A; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE EXPRESSION; INFLAMMATION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIAL PROTEINS; CARBOXYLIC ESTER HYDROLASES; CYTOKINES; GENE EXPRESSION PROFILING; IMMUNOBLOTTING; MACROPHAGES; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NF-KAPPA B; NITRIC OXIDE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOCOCCUS PNEUMONIAE; VIRULENCE FACTORS;

STREPTOCOCCUS PNEUMONIAE;

EID: 70349515022     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2009.07.002     Document Type: Article

References (40)

1. Tai S.S. Streptococcus pneumoniae protein vaccine candidates: properties, activities and animal studies. Crit Rev Microbiol 32 (2006) 139-153
2. Siber G.R. Pneumococcal disease: prospects for a new generation of vaccines. Science 265 (1994) 1385-1387
3. Alonsodevelasco E., Verheul A.F.M., Verhoef J., and Snippe H. Streptococcus pneumonia: virulence factors, pathogenesis, and vaccines. Microbiol Rev 59 (1995) 591-603
4. Catterall J.R. Streptococcus pneumonia. Thorax 54 (1999) 929-937
5. Hava D.L., and Camilli A. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45 (2002) 1389-1406
6. Schumann R.R., Pfeil D., Freyer D., Buerger W., Lamping N., Kirschning C.J., et al. Lipopolysaccharide and pneumococcal cell wall components activate the mitogen activated protein kinases (MAPK) erk-1, erk-2, and p38 in astrocytes. Glia 22 (1998) 295-305
7. Braun J.S., Novak R., Gao G., Murray P.J., and Shenep J.L. Pneumolysin, a protein toxin of Streptococcus pneumoniae, induces nitric oxide production from macrophages. Infect Immun 67 (1999) 3750-3756
8. Um S.H., Son E.W., Kim BoMoon E.Y., Rhee D.K., and Pyo S. Activation of murine peritoneal macrophages by Streptococcus pneumoniae type II capsular polysaccharide: involvement of CD14-dependent pathway. Scand J Immunol 52 (2000) 39-45
9. Shoma S., Tsuchiya K., Kawamura I., Nomura T., Hara H., Uchiyama R., et al. Critical involvement of pneumolysin in production of interleukin-1 and caspase-1-dependent cytokines in infection with Streptococcus pneumonia in vitro: a novel function of pneumolysin in caspase-1 activation. Infect Immun (2008) 10.1128/IAI.01269-07
10. Blue C.E., Paterson G.K., Kerr A.R., Berge M., Claverys J.P., and Mitchell T.J. ZmpB, a novel virulence factor of Streptococcus pneumoniae that induces tumor necrosis factor alpha production in the respiratory tract. Infect Immun 71 (2003) 4925-4935
11. Kim M.H., Kang B.S., Kim S., Kim K.J., Lee C.H., Oh B.C., et al. The crystal structure of the EstA protein, a virulence factor from Streptococcus pneumoniae. Proteins 70 (2007) 578-583
12. Bruyn G.A., Zegers B.J., and Furth R.V. Mechanisms of host defense against infection with Streptococcus pneumoniae. Clin Infect Dis 14 (1992) 251-262
13. Knapp S., Leemans J.C., Florquin S., Branger J., Maris N.A., Pater J., et al. Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am J Respir Crit Care Med 167 (2003) 171-179
14. Amory-Rivier C.F., Mohler J., Bé dos J.P., Dupuis E.A., Henin D., Joly M.M., et al. Nuclear factor-κB activation in mouse lung lavage cells in response to Streptococcus pneumoniae pulmonary infection. Crit Care Med 28 (2000) 3249-3256
15. Korhonen R., Lahti A., Kankaanranta H., and Moilanen E. Nitric oxide production and signaling in inflammation. Curr Drug Targets 4 (2005) 471-479
16. De Stefano D., Maiuri M.C., Iovine B., Ialenti A., Bevilacqua M.A., and Carnuccio R. The role of NF-kappaB, IRF-1, and STAT-1alpha transcription factors in the iNOS gene induction by gliadin and IFN-gamma in RAW 264.7 macrophages. J Mol Med 84 (2006) 65-74
17. Mogensen T.H., Berg R.S., Østergaard L., and Paludan S.R. Streptococcus pneumoniae stabilizes tumor necrosis factor α mRNA through a pathway dependent on p38 MAPK but independent of Toll-like receptors. BMC Immunol (2008) 10.1186/1471-2172-9-52
18. Schmeck B., Zahlten J., Moog K., Van Laak V., Huber S., Hocke A.C., et al. Streptococcus pneumoniae-induced p38 MAPK-dependent phosphorylation of RelA at the interleukin-8 promotor. J Biol Chem 279 (2004) 53241-53247
19. Shishodia S., and Aggarwal B.B. Nuclear factor-kappaB: a friend or a foe in cancer?. Biochem Pharmacol 68 (2004) 1071-1080
20. Bandyopadhaya A., Sarkar M., and Chaudhuri K. IL-1β expression in Int407 is induced by flagellin of Vibrio cholerae through TLR5 mediated pathway. Microb Pathog (2008) 10.1016/j.micpath.2008.01.004
21. N'Guessan P.D., Hippenstiel S., Etouem M.O., Zahlten J., Beermann W., Lindner D., et al. Streptococcus pneumoniae induced p38 MAPK- and NF-kappaB-dependent COX-2 expression in human lung epithelium. Am J Physiol Lung Cell Mol Physiol 290 (2006) 1131-1138
22. Monier R.M., Orman K.L., Meals E.A., and English B.K. Differential effects of p38- and extracellular signal-regulated kinase mitogen-activated protein kinase inhibitors on inducible nitric oxide synthase and tumor necrosis factor production in murine macrophages stimulated with Streptococcus pneumoniae. J Infect Dis 185 (2002) 921-926
23. Ajizian S.J., English B.K., and Meals E.A. Specific inhibitors of p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways block inducible nitric oxide synthase and tumor necrosis factor accumulation in murine macrophages stimulated with lipopolysaccharide and interferon-gamma. J Infect Dis 179 (1999) 939-944
24. Cary S.P., Winger J.A., Derbyshire E.R., and Marletta M.A. Nitric oxide signaling: no longer simply on or off. Trends Biochem Sci 31 (2006) 231-239
25. Marriott H.M., Ali F., Read R.C., Mitchell T.J., Whyte M.K., and Dockrell D.H. Nitric oxide levels regulate macrophage commitment to apoptosis or necrosis during pneumococcal infection. FASEB J 18 (2004) 1126-1128
26. Wolkow P.P. Involvement and dual effects of nitric oxide in septic shock. Inflamm Res 47 (1998) 152-166
27. Bonizzi G., and Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25 (2004) 280-288
28. Finco T.S., and Baldwin A.S. Mechanistic aspects of NF-kappa B regulation. The emerging role of phosphorylation and proteolysis. Immunity 3 (1995) 263-272
29. Ronning D.R., Klabunde T., Besra G.S., Vissa V.D., Belisle J.T., and Sacchettini J.C. Crystal structure of the secreted form of antigen 85C reveals potential targets for mycobacterial drugs and vaccines. Nat Struct Biol 7 (2000) 141-146
30. Schubot F.D., Kataeva I.A., Blum D.L., Shah A.K., Ljungdahl L.G., Rose J.P., et al. Structural basis for the substrate specificity of the feruloyl esterase domain of the cellulosomal xylanase Z from Clostridium thermocellum. Biochemistry 40 (2001) 12524-12532
31. Bergeron Y.N., Ouellet M., Olivier S.M., and Bergeron M.G. Immunomodulation of pneumococcal pulmonary infection with N(G)-monomethyl-l-arginine. Antimicrob Agents Chemother 43 (1999) 2283-2290
32. Bernatowicz A., Kodel U., Frei K., Fontana A., and Pfister H.W. Production of nitrite by primary rat astrocytes in response to pneumococci. J Neuroimmunol 60 (1995) 53-61
33. Destache C.J., Pakiz C.B., Dash A.K., and Larsen C. Nitric oxide concentrations and cerebrospinal fluid parameters in an experimental animal model of Streptococcus pneumoniae meningitis. Pharmacotherapy 18 (1998) 612-619
34. Freyer D., Weih M., Weber J.R., Burger W., Scholz P., Manz R., et al. Pneumococcal cell wall components induce nitric oxide synthase and TNF-alpha in astroglial-enriched cultures. Glia 16 (1996) 1-6
35. Kerr A.R., Wei X.Q., Andrew P.W., and Mitchell T.J. Nitric oxide exerts distinct effects in local and systemic infections with Streptococcus pneumoniae. Microb Pathog 36 (2004) 303-310
36. Riesenfeld-Orn I., Wolpe S., Garcia-Bustos J.F., Hoffmann M.K., and Tuomanen E. Production of interleukin-1 but not tumor necrosis factor by human monocytes stimulated with pneumococcal cell surface components. Infect Immun 57 (1989) 1890-1893
37. Wilson M., Reddi K., and Henderson B. Cytokine-inducing components of periodontopathogenic bacteria. J Periodontal Res 31 (1996) 393-407
38. Ogunniyi A.D., LeMessurier K.S., Graham R.M.A., Watt J.M., Briles D.E., Stroeher U.H., et al. Contributions of pneumolysin, pneumococcal surface protein A (PspA), and PspC to pathogenicity of Streptococcus pneumoniae D39 in a mouse model. Infect Immun (2007) 10.1128/IAI.01384-06
39. Houldsworth S., Andrew P.W., and Mitchell T.J. Pneumolysin stimulates production of tumor necrosis factor alpha and interleukin-13 by human mononuclear phagocytes. Infect Immun 62 (1994) 1501-1503
40. Kweon S.M., Wang B., Rixter D., Lim J.H., Koga T., Ishinaga H., et al. Synergistic activation of NF-kappaB by nontypeable H. influenzae and S. pneumoniae is mediated by CK2, IKKbeta-IkappaBalpha, and p38 MAPK. Biochem Biophys Res Commun 351 (2006) 368-375