Central role of manganese in regulation of stress responses, physiology, and metabolism in Streptococcus pneumoniae

Journal of Bacteriology

Volumn 192, Issue 17, 2010, Pages 4489-4497

  Ogunniyi, Abiodun D ^a   Mahdi, Layla K ^a   Jennings, Michael P ^b   McEwan, Alastair G ^c   McDevitt, Christopher A ^a   Van Der Hoek, Mark B ^a   Bagley, Christopher J ^a   Hoffmann, Peter ^a   Gould, Katherine A ^d   Paton, James C ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC PERMEASE; BACTERIAL ANTIGEN; GENE PRODUCT; MANGANESE; OLIGOPEPTIDE; PERMEASE; PHOSPHOGLUCONATE DEHYDROGENASE; PNEUMOCOCCAL SURFACE ANTIGEN A; PROTEIN SODA; PROTEIN SPXB; PROTEOME; TRANSCRIPTOME; UNCLASSIFIED DRUG; ADHESIN; BACTERIAL PROTEIN; LIPOPROTEIN; PSAA PROTEIN, STREPTOCOCCUS;

ADHC GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BINDING AFFINITY; CZCD GENE; DELETION MUTANT; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE CLUSTER; NITROSATIVE STRESS; NMLR GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PCPA GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; PRTA GENE; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTOMICS; UPREGULATION; WILD TYPE; CULTURE MEDIUM; DNA MICROARRAY; DRUG EFFECT; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

STREPTOCOCCUS PNEUMONIAE;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; CULTURE MEDIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; LIPOPROTEINS; MANGANESE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PROTEOME; STREPTOCOCCUS PNEUMONIAE;

EID: 77956505339     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00064-10     Document Type: Article

References (58)

1. Alkhuder, K., K. L. Meibom, I. Dubail, M. Dupuis, and A. Charbit. 2009. Glutathione provides a source of cysteine essential for intracellular multiplication of Francisella tularensis. PLoS Pathog. 5:e1000284.
2. Anjem, A., S. Varghese, and J. A. Imlay. 2009. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 72:844-858.
3. Avery, O. T., C. M. MacLeod, and M. McCarty. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Inductions of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79:137-158.
4. Berry, A. M., and J. C. Paton. 1996. Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect. Immun. 64:5255-5262.
5. Brown, A. T., and C. L. Wittenberger. 1971. Mechanism for regulating the distribution of glucose carbon between the Embden-Meyerhof and hexosemonophosphate pathways in Streptococcus faecalis. J. Bacteriol. 106:456-467.
6. Chicharro, J. L., V. Serrano, R. Urena, A. M. Gutierrez, A. Carvajal, P. Fernandez-Hernando, and A. Lucia. 1999. Trace elements and electrolytes in human resting mixed saliva after exercise. Br. J. Sports Med. 33:204-207.
7. Corbin, B. D., E. H. Seeley, A. Raab, J. Feldmann, M. R. Miller, V. J. Torres, K. L. Anderson, B. M. Dattilo, P. M. Dunman, R. Gerads, R. M. Caprioli, W. Nacken, W. J. Chazin, and E. P. Skaar. 2008. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319:962-965.
8. Del Corso, A., M. Cappiello, F. Buono, R. Moschini, A. Paolicchi, and U. Mura. 2006. Colorimetric coupled enzyme assay for gamma-glutamyltransferase activity using glutathione as substrate. J. Biochem. Biophys. Methods 67:123-130.
9. Dintilhac, A., G. Alloing, C. Granadel, and J. P. Claverys. 1997. Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol. Microbiol. 25:727-739.
10. Eggleston, L. V., and H. A. Krebs. 1974. Regulation of the pentose phosphate cycle. Biochem. J. 138:425-435.
11. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
12. Encheva, V., S. E. Gharbia, R. Wait, S. Begum, and H. N. Shah. 2006. Comparison of extraction procedures for proteome analysis of Streptococcus pneumoniae and a basic reference map. Proteomics 6:3306-3317.
13. Eriksson, L., E. Johansson, N. Kettaneh-Wold, and S. Wold. 2001. Multiand megavariate data analysis: principles and applications. Umetrics Academy, Umeå, Sweden.
14. Fahey, R. C., W. C. Brown, W. B. Adams, and M. B. Worsham. 1978. Occurrence of glutathione in bacteria. J. Bacteriol. 133:1126-1129.
15. Glasfeld, A., E. Guedon, J. D. Helmann, and R. G. Brennan. 2003. Structure of the manganese-bound manganese transport regulator of Bacillus subtilis. Nat. Struct. Biol. 10:652-657.
16. Hendriksen, W. T., H. J. Bootsma, A. van Diepen, S. Estevao, O. P. Kuipers, R. de Groot, and P. W. Hermans. 2009. Strain-specific impact of PsaR of Streptococcus pneumoniae on global gene expression and virulence. Microbiology 155:1569-1579.
17. Hirst, R. A., A. Kadioglu, C. O'Callaghan, and P. W. Andrew. 2004. The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin. Exp. Immunol. 138:195-201.
18. 2+-dependent regulation of multiple genes in Streptococcus pneumoniae through PsaR and the resultant impact on virulence. Infect. Immun. 74:1171-1180.
19. Johnston, J. W., L. E. Myers, M. M. Ochs, W. H. Benjamin, Jr., D. E. Briles, and S. K. Hollingshead. 2004. Lipoprotein PsaA in virulence of Streptococcus pneumoniae: surface accessibility and role in protection from superoxide. Infect. Immun. 72:5858-5867.
20. Kehres, D. G., and M. E. Maguire. 2003. Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol. Rev. 27:263-290.
21. Kidd, S. P., D. Jiang, M. P. Jennings, and A. G. McEwan. 2007. Glutathione-dependent alcohol dehydrogenase AdhC is required for defense against nitrosative stress in Haemophilus influenzae. Infect. Immun. 75:4506-4513.
22. 2+-resistance gene czcD in Streptococcus pneumoniae. Mol. Microbiol. 65:1049-1063.
23. 2+ on PsaRmediated expression of the virulence genes pcpA, prtA, and psaBCA of Streptococcus pneumoniae. J. Bacteriol. 190:5382-5393.
24. Knapp, S., J. C. Leemans, S. Florquin, J. Branger, N. A. Maris, J. Pater, N. van Rooijen, and T. van der Poll. 2003. Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 167:171-179.
25. Krab, I. M., and A. Parmeggiani. 1998. EF-Tu, a GTPase odyssey. Biochim. Biophys. Acta 1443:1-22.
26. Krachler, M., E. Rossipal, and D. Micetic-Turk. 1999. Concentrations of trace elements in sera of newborns, young infants, and adults. Biol. Trace Elem. Res. 68:121-135.
27. Lacks, S., and R. D. Hotchkiss. 1960. A study of the genetic material determining an enzyme in Pneumococcus. Biochim. Biophys. Acta 39:508-518.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lawrence, M. C., P. A. Pilling, V. C. Epa, A. M. Berry, A. D. Ogunniyi, and J. C. Paton. 1998. The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6:1553-1561.
30. LeMessurier, K. S., A. D. Ogunniyi, and J. C. Paton. 2006. Differential expression of key pneumococcal virulence genes in vivo. Microbiology. 152:305-311.
31. -ΔΔCT Method. Methods 25:402-408.
32. Loisel, E., L. Jacquamet, L. Serre, C. Bauvois, J. L. Ferrer, T. Vernet, A. M. Di Guilmi, and C. Durmort. 2008. AdcAII, a new pneumococcal Zn-binding protein homologous with ABC transporters: biochemical and structural analysis. J. Mol. Biol. 381:594-606.
33. Marra, A., S. Lawson, J. S. Asundi, D. Brigham, and A. E. Hromockyj. 2002. In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection. Microbiology. 148:1483-1491.
34. McAllister, L. J., H. J. Tseng, A. D. Ogunniyi, M. P. Jennings, A. G. McEwan, and J. C. Paton. 2004. Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol. Microbiol. 53:889-901.
35. McCluskey, J., J. Hinds, S. Husain, A. Witney, and T. J. Mitchell. 2004. A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae. Mol. Microbiol. 51:1661-1675.
36. Melkani, G. C., R. L. Sielaff, G. Zardeneta, and J. A. Mendoza. 2008. Divalent cations stabilize GroEL under conditions of oxidative stress. Biochem. Biophys. Res. Commun. 368:625-630.
37. Novak, R., J. S. Braun, E. Charpentier, and E. Tuomanen. 1998. Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa. Mol. Microbiol. 29:1285-1296.
38. Ogunniyi, A. D., P. Giammarinaro, and J. C. Paton. 2002. The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo. Microbiology 148:2045-2053.
39. Overweg, K., C. D. Pericone, G. G. Verhoef, J. N. Weiser, H. D. Meiring, A. P. De Jong, R. De Groot, and P. W. Hermans. 2000. Differential protein expression in phenotypic variants of Streptococcus pneumoniae. Infect. Immun. 68:4604-4610.
40. Papp-Wallace, K. M., and M. E. Maguire. 2006. Manganese transport and the role of manganese in virulence. Annu. Rev. Microbiol. 60:187-209.
41. Pastore, A., R. Massoud, C. Motti, A. Lo Russo, G. Fucci, C. Cortese, and G. Federici. 1998. Fully automated assay for total homocysteine, cysteine, cysteinylglycine, glutathione, cysteamine, and 2-mercaptopropionylglycine in plasma and urine. Clin. Chem. 44:825-832.
42. Pastore, A., F. Piemonte, M. Locatelli, A. Lo Russo, L. M. Gaeta, G. Tozzi, and G. Federici. 2001. Determination of blood total, reduced, and oxidized glutathione in pediatric subjects. Clin. Chem. 47:1467-1469.
43. Paton, J. C. 1998. Novel pneumococcal surface proteins: role in virulence and vaccine potential. Trends Microbiol. 6:85-87. (Discussion, 6:87-88.)
44. Rawlings, N. D., and A. J. Barrett. 1993. Evolutionary families of peptidases. Biochem. J. 290(Pt. 1):205-218.
45. Rigali, S., A. Derouaux, F. Giannotta, and J. Dusart. 2002. Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J. Biol. Chem. 277:12507-12515.
46. Rogers, T. J., A. W. Paton, S. R. McColl, and J. C. Paton. 2003. Enhanced CXC chemokine responses of human colonic epithelial cells to locus of enterocyte effacement-negative shiga-toxigenic Escherichia coli. Infect. Immun. 71:5623-5632.
47. Russell, H., J. A. Tharpe, D. E. Wells, E. H. White, and J. E. Johnson. 1990. Monoclonal antibody recognizing a species-specific protein from Streptococcus pneumoniae. J. Clin. Microbiol. 28:2191-2195.
48. Scheuhammer, A. M., and M. G. Cherian. 1985. Binding of manganese in human and rat plasma. Biochim. Biophys. Acta 840:163-169.
49. Smyth, G. K. 2005. Limma: linear models for microarray data, p. 397-420. In V. Carey, R. Gentleman, S. Dudoit, R. Irizarry, and W. Huber (ed.), Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, NY.
50. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:Article3.
51. Smyth, G. K., and T. Speed. 2003. Normalization of cDNA microarray data. Methods 31:265-273.
52. St. Croix, C. M., K. Leelavaninchkul, S. C. Watkins, V. E. Kagan, and B. R. Pitt. 2005. Nitric oxide and zinc homeostasis in acute lung injury. Proc. Am. Thorac. Soc. 2:236-242.
53. Stroeher, U. H., S. P. Kidd, S. L. Stafford, M. P. Jennings, J. C. Paton, and A. G. McEwan. 2007. A pneumococcal MerR-like regulator and S-nitroso-glutathione reductase are required for systemic virulence. J. Infect. Dis. 196:1820-1826.
54. Taniai, H., K. Iida, M. Seki, M. Saito, S. Shiota, H. Nakayama, and S. Yoshida. 2008. Concerted action of lactate oxidase and pyruvate oxidase in aerobic growth of Streptococcus pneumoniae: role of lactate as an energy source. J. Bacteriol. 190:3572-3579.
55. Tettelin, H., K. E. Nelson, I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, J. Heidelberg, R. T. DeBoy, D. H. Haft, R. J. Dodson, A. S. Durkin, M. Gwinn, J. F. Kolonay, W. C. Nelson, J. D. Peterson, L. A. Umayam, O. White, S. L. Salzberg, M. R. Lewis, D. Radune, E. Holtzapple, H. Khouri, A. M. Wolf, T. R. Utterback, C. L. Hansen, L. A. McDonald, T. V. Feldblyum, S. Angiuoli, T. Dickinson, E. K. Hickey, I. E. Holt, B. J. Loftus, F. Yang, H. O. Smith, J. C. Venter, B. A. Dougherty, D. A. Morrison, S. K. Hollingshead, and C. M. Fraser. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.
56. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76:4350-4354.
57. Tseng, H. J., A. G. McEwan, J. C. Paton, and M. P. Jennings. 2002. Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect. Immun. 70:1635-1639.
58. Yesilkaya, H., A. Kadioglu, N. Gingles, J. E. Alexander, T. J. Mitchell, and P. W. Andrew. 2000. Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect. Immun. 68:2819-2826.