Glutamate utilization promotes meningococcal survival in vivo through avoidance of the neutrophil oxidative burst

Molecular Microbiology

Volumn 81, Issue 5, 2011, Pages 1330-1342

  Talà, Adelfia ^a   Monaco, Caterina ^a   Nagorska, Krzysztofa ^b   Exley, Rachel M ^b   Corbett, Anne ^b   Zychlinsky, Arturo ^c   Alifano, Pietro ^a   Tang, Christoph M ^b  

^a UNIVERSITY OF SALENTO   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; GLUTATHIONE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE;

AMINO ACID TRANSPORT; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; CYTOLYSIS; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NEISSERIA MENINGITIDIS; NEUTROPHIL; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; RESPIRATORY BURST; SIALYLATION;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; BACTEREMIA; BACTERIAL PROTEINS; GLUTAMIC ACID; GLUTATHIONE; HYDROGEN PEROXIDE; MENINGOCOCCAL INFECTIONS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEISSERIA MENINGITIDIS; NEUTROPHILS; OXIDATIVE STRESS; PHAGOCYTOSIS; RATS; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS;

EID: 80051934372     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07766.x     Document Type: Article

References (69)

1. Andersen, L.P., Blom, J., and Nielsen, H. (1993) Survival and ultrastructural changes of Helicobacter pylori after phagocytosis by human polymorphonuclear leukocytes and monocytes. APMIS 101: 61-72.
2. Bouter, S., Kerklaan, P.R., Zoetemelk, C.E., and Mohn, G.R. (1988) Biochemical characterization of glutathione-deficient mutants of Escherichia coli K12 and Salmonella strains TA1535 and TA100. Biochem Pharmacol 37: 577-581.
3. Brandtzaeg, P., Ovstebo, R., and Kierulf, P. (1995) Bacteremia and compartmentalization of LPS in meningococcal disease. Prog Clin Biol Res 392: 219-233.
4. Carmel-Harel, O., and Storz, G. (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54: 439-461.
5. Carpenter, E.P., Corbett, A., Thomson, H., Adacha, J., Jensen, K., Bergeron, J., etal. (2007) AP endonuclease paralogues with distinct activities in DNA repair and bacterial pathogenesis. EMBO J 26: 1363-1372.
6. Catlin, B.W. (1973) Nutritional profiles of Neisseria gonorrhoeae, Neisseria meningitidis, and Neisseria lactamica in chemically defined media and the use of growth requirements for gonococcal typing. J Infect Dis 128: 178-194.
7. Christodoulides, M., Everson, J.S., Liu, B.L., Lambden, P.R., Watt, P.J., Thomas, E.J., and Heckels, J.E. (2000) Interaction of primary human endometrial cells with Neisseria gonorrhoeae expressing green fluorescent protein. Mol Microbiol 35: 32-43.
8. Colicchio, R., Pagliarulo, C., Lamberti, F., Vigliotta, G., Bruni, C.B., Alifano, P., and Salvatore, P. (2006) RecB-dependent mutator phenotype in Neisseria meningitidis strains naturally defective in mismatch repair. DNA Repair (Amst) 5: 1428-1438.
9. Colicchio, R., Ricci, S., Lamberti, F., Pagliarulo, C., Pagliuc, C., Braione, V., etal. (2009) The meningococcal ABC-type L-gutamate transporter GltT is necessary for the development of experimental meningitidis in mice. Infect Immun 77: 3578-3587.
10. Collard, C.D., Park, K.A., Montalto, M.C., Alapati, S., Buras, J.A., Stahl, G.L., and Colgan, S.P. (2002) Neutrophil-derived glutamate regulates vascular endothelial barrier function. J Biol Chem 277: 14801-14811.
11. Criss, A.K., and Seifert, H.S. (2008) Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes. Cell Microbiol 10: 2257-2270.
12. Darton, T., Guiver, M., Naylor, S., Jack, D.L., Kaczmarski, E.B., Borrow, R., and Read, R.C. (2008) Severity of meningococcal disease associated with genomic bacterial load. Clin Infect Dis 48: 587-594.
13. DeLeo, F.R., Allen, L.A., Apicella, M., and Nauseef, W.M. (1999) NADPH oxidase activation and assembly during phagocytosis. J Immunol 163: 6732-6740.
14. van Deuren, M., Brandtzaeg, P., and van der Meer, J.W. (2000) Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13: 144-166.
15. Divino Filho, J.C., Hazel, S.J., Furst, P., Bergstrom, J., and Hall, K. (1998) Glutamate concentration in plasma, erythrocyte and muscle in relation to plasma levels of insulin-like growth factor (IGF)-I, IGF binding protein-1 and insulin in patients on haemodialysis. J Endocrinol 156: 519-527.
16. Dunn, K.L., Farrant, J.L., Langford, P.R., and Kroll, J.S. (2003) Bacterial [Cu, Zn]-cofactored superoxide dismutase protects opsonized, encapsulated Neisseria meningitidis from phagocytosis by human monocytes/macrophages. Infect Immun 71: 1604-1607.
17. Echenique-Rivera, H., Muzzi, A., Del Tordello, E., Seib, K.L., Francois, P., Rappuoli, R., etal. (2011) Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival. PLoS Pathog 7: e1002027.
18. Estabrook, M.M., Zhou, D., and Apicella, M.A. (1998) Nonopsonic phagocytosis of group C Neisseria meningitidis by human neutrophils. Infect Immun 66: 1028-1036.
19. Exley, R.M., Shaw, J., Mowe, E., Sun, Y.H., West, N.P., Williamson, M., etal. (2005) Available carbon source influences the resistance of Neisseria meningitidis against complement. J Exp Med 201: 1637-1645.
20. Fang, F.C. (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2: 820-832.
21. Figueroa, J.E., and Densen, P. (1991) Infectious diseases associated with complement deficiencies. Clin Microbiol Rev 4: 359-395.
22. Fijen, C.A., Bredius, R.G., Kuijper, E.J., Out, T.A., De Haas, M., De Wit, A.P., etal. (2000) The role of Fcgamma receptor polymorphisms and C3 in the immune defence against Neisseria meningitidis in complement-deficient individuals. Clin Exp Immunol 120: 338-345.
23. Fuchs, T.A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., etal. (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176: 231-241.
24. Geoffroy, M.C., Floquet, S., Metais, A., Nassif, X., and Pelicic, V. (2003) Large-scale analysis of the meningococcus genome by gene disruption: resistance to complement-mediated lysis. Genome Res 13: 391-398.
25. Guarner, J., Greer, P.W., Whitney, A., Shieh, W.J., Fischer, M., White, E.H., etal. (2004) Pathogenesis and diagnosis of human meningococcal disease using immunohistochemical and PCR assays. Am J Clin Pathol 122: 754-764.
26. Hammerschmidt, S., Birkholz, C., Zahringer, U., Robertson, B.D., van Putten, J., Ebeling, O., and Frosch, M. (1994) Contribution of genes from the capsule gene complex (cps) to lipooligosaccharide biosynthesis and serum resistance in Neisseria meningitidis. Mol Microbiol 11: 885-896.
27. Hampton, M.B., Kettle, A.J., and Winterbourn, C.C. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017.
28. Haralambous, E., Dolly, S.O., Hibberd, M.L., Litt, D.J., Udalova, I.A., O'Dwyer, C., etal. (2006) Factor H, a regulator of complement activity, is a major determinant of meningococcal disease susceptibility in UK Caucasian patients. Scand J Infect Dis 38: 764-771.
29. Hendriksen, W.T., Kloosterman, T.G., Bootsma, H.J., Estevao, S., de Groot, R., Kuipers, O.P., and Hermans, P.W. (2008) Site-specific contributions of glutamine-dependent regulator GlnR and GlnR-regulated genes to virulence of Streptococcus pneumoniae. Infect Immun 76: 1230-1238.
30. Hill, J.C. (1971) Effect of glutamate on exogenous citrate catabolism of Neisseria meningitidis and of other species of Neisseria. J Bacteriol 106: 819-823.
31. Imlay, J.A. (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776.
32. Jang, D.S., Kang, B.S., Ryu, S.Y., Chang, I.M., Min, K.R., and Kim, Y. (1999) Inhibitory effects of resveratrol analogs on unopsonized zymosan-induced oxygen radical production. Biochem Pharmacol 57: 705-712.
33. Kobayashi, S.D., Braughton, K.R., Whitney, A.R., Voyich, J.M., Schwan, T.G., Musser, J.M., and DeLeo, F.R. (2003) Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci USA 100: 10948-10953.
34. Li, M.S., Chow, N.Y., Sinha, S., Halliwell, D., Finney, M., Gorringe, A.R., etal. (2009) A Neisseria meningitidis NMB1966 mutant is impaired for invasion of respiratory epithelial cells, survival in human blood and for virulence in vivo. Med Microbiol Immunol 198: 57-67.
35. McCaw, S.E., Schneider, J., Liao, E.H., Zimmermann, W., and Gray-Owen, S.D. (2003) Immunoreceptor tyrosine-based activation motif phosphorylation during engulfment of Neisseria gonorrhoeae by the neutrophil-restricted CEACAM3 (CD66d) receptor. Mol Microbiol 49: 623-637.
36. McNeil, G., and Virji, M. (1997) Phenotypic variants of meningococci and their potential in phagocytic interactions: the influence of opacity proteins, pili, PilC and surface sialic acids. Microb Pathog 22: 295-304.
37. Madico, G., Welsch, J.A., Lewis, L.A., McNaughton, A., Perlman, D.H., Costello, C.E., etal. (2006) The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol 177: 501-510.
38. Mallavia, L.P., and Weiss, E. (1970) Catabolic activities of Neisseria meningitidis: utilization of glutamate. J Bacteriol 101: 127-132.
39. Mandrell, R.E., McLaughlin, R., Aba Kwaik, Y., Lesse, A., Yamasaki, R., Gibson, B., etal. (1992) Lipooligosaccharides (LOS) of some Haemophilus species mimic human glycosphingolipids, and some LOS are sialylated. Infect Immun 60: 1322-1328.
40. Monaco, C., Tala, A., Spinosa, M.R., Progida, C., De Nitto, E., Gaballo, A., etal. (2006) Identification of a meningococcal l-glutamate ABC transporter operon essential for growth in low-sodium environments. Infect Immun 74: 1725-1740.
41. Moore, T.D., and Sparling, P.F. (1996) Interruption of the gpxA gene increases the sensitivity of Neisseria meningitidis to paraquat. J Bacteriol 178: 4301-4305.
42. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182.
43. Ovstebo, R., Brandtzaeg, P., Brusletto, B., Haug, K.B., Lande, K., Hoiby, E.A., and Kierulf, P. (2004) Use of robotized DNA isolation and real-time PCR to quantify and identify close correlation between levels of Neisseria meningitidis DNA and lipopolysaccharides in plasma and cerebrospinal fluid from patients with systemic meningococcal disease. J Clin Microbiol 42: 2980-2987.
44. Pagliarulo, C., Salvatore, P., De Vitis, L.R., Colicchio, R., Monaco, C., Tredici, M., etal. (2004) Regulation and differential expression of gdhA encoding NADP-specific glutamate dehydrogenase in Neisseria meningitidis clinical isolates. Mol Microbiol 51: 1757-1772.
45. Parkhill, J., Achtman, M., James, K.D., Bentley, S.D., Churcher, C., Klee, S.R., etal. (2000) Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404: 502-506.
46. Read, R.C., Zimmerli, S., Broaddus, C., Sanan, D.A., Stephens, D.S., and Ernst, J.D. (1996) The (alpha2->8)-linked polysialic acid capsule of group B Neisseria meningitidis modifies multiple steps during interaction with human macrophages. Infect Immun 64: 3210-3217.
47. Reitzer, L. (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57: 155-176.
48. Schneider, M.C., Exley, R.M., Chan, H., Feavers, I., Kang, Y.H., Sim, R.B., and Tang, C.M. (2006) Functional significance of factor H binding to Neisseria meningitidis. J Immunol 176: 7566-7575.
49. Schneider, M.C., Exley, R.M., Ram, S., Sim, R.B., and Tang, C.M. (2007) Interactions between Neisseria meningitidis and the complement system. Trends Microbiol 15: 233-240.
50. Schneider, M.C., Prosser, B.E., Caesar, J.J., Kugelberg, E., Li, S., Zhang, Q., etal. (2009) Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature 16: 890-893.
51. Segal, A.W. (1996) The NADPH oxidase and chronic granulomatous disease. Mol Med Today 2: 129-135.
52. Seib, K.L., Tseng, H.J., McEwan, A.G., Apicella, M.A., and Jennings, M.P. (2004) Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J Infect Dis 190: 136-147.
53. Shibayama, K., Wachino, J., Arakawa, Y., Saidijam, M., Rutherford, N.G., and Henderson, P.J. (2007) Metabolism of glutamine and glutathione via gamma-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol Microbiol 64: 396-406.
54. Simons, M.P., Nauseef, W.M., and Apicella, M.A. (2005) Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect Immun 73: 1971-1977.
55. Simons, M.P., Nauseef, W.M., Griffith, T.S., and Apicella, M.A. (2006) Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell Microbiol 8: 1780-1790.
56. Soler-Garcia, A.A., and Jerse, A.E. (2004) A Neisseria gonorrhoeae catalase mutant is more sensitive to hydrogen peroxide and paraquat, an inducer of toxic oxygen radicals. Microb Pathog 37: 55-63.
57. Stephens, D.S., Greenwood, B., and Brandtzaeg, P. (2007) Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369: 2196-2210.
58. Sun, Y.H., Bakshi, S., Chalmers, R., and Tang, C.M. (2000) Functional genomics of Neisseria meningitidis pathogenesis. Nat Med 6: 1269-1273.
59. Tala, A., De Stefano, M., Bucci, C., and Alifano, P. (2008) Reverse transcriptase-PCR differential display analysis of meningococcal transcripts during infection of human cells: up-regulation of priA and its role in intracellular replication. BMC Microbiol 8: 131.
60. Tettelin, H., Saunders, N.J., Heidelberg, J., Jeffries, A.C., Nelson, K.E., Eisen, J.A., etal. (2000) Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287: 1809-1815.
61. Thomas, E.L. (1984) Disulfide reduction and sulfhydryl uptake by Streptococcus mutans. J Bacteriol 157: 240-246.
62. Tzeng, Y.L., Ambrose, K.D., Zughaier, S., Zhou, X., Miller, Y.K., Shafer, W.M., and Stephens, D.S. (2005) Cationic antimicrobial peptide resistance in Neisseria meningitidis. J Bacteriol 187: 5387-5396.
63. Unkmeir, A., Kammerer, U., Stade, A., Hubner, C., Haller, S., Kolb-Maurer, A., etal. (2002) Lipooligosaccharide and polysaccharide capsule: virulence factors of Neisseria meningitidis that determine meningococcal interaction with human dendritic cells. Infect Immun 70: 2454-2462.
64. Urban, C.F., Lourido, S., and Zychlinsky, A. (2006) How do microbes evade neutrophil killing? Cell Microbiol 8: 1687-1696.
65. Veale, D.R., Goldner, M., Penn, C.W., Ward, J., and Smith, H. (1979) The intracellular survival and growth of gonococci in human phagocytes. J Gen Microbiol 113: 383-393.
66. Virji, M., Makepeace, K., Ferguson, D.J., and Watt, S.M. (1996) Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic neisseriae. Mol Microbiol 22: 941-950.
67. Vogel, U., and Frosch, M. (1999) Mechanisms of neisserial serum resistance. Mol Microbiol 32: 1133-1139.
68. Weichselbaum, A. (1887) Ueber die Aetiologie der akuten Meningitis Cerebrospinalis. Fortschrift Medizin 5: 573-587.
69. Yazdankhah, S.P., and Caugant, D.A. (2004) Neisseria meningitidis: an overview of the carriage state. J Med Microbiol 53: 821-832.