The Effects of Methionine Acquisition and Synthesis on Streptococcus Pneumoniae Growth and Virulence

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Basavanna, Shilpa ^a   Chimalapati, Suneeta ^b   Maqbool, Abbas ^c   Rubbo, Bruna ^b   Yuste, Jose ^d   Wilson, Robert J ^b   Hosie, Arthur ^e   Ogunniyi, Abiodun D ^f   Paton, James C ^f   Thomas, Gavin ^c   Brown, Jeremy S ^b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^c UNIVERSITY OF YORK   (United Kingdom)

^d CSIC   (Spain)

^e UNIVERSITY OF BEDFORDSHIRE   (United Kingdom)

^f UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN G; METHIONINE; PNEUMOCOCCUS VACCINE; PROTEIN METQ; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BINDING AFFINITY; COLONY FORMING UNIT; CONTROLLED STUDY; GENE DELETION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; METE GENE; METF GENE; METQ GENE; MIXED INFECTION; MOUSE; NASOPHARYNX; NONHUMAN; PNEUMOCOCCAL INFECTION; STREPTOCOCCUS PNEUMONIAE; VACCINATION; WILD TYPE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BACTERIAL VACCINES; BIOLOGICAL TRANSPORT; GENETIC LOCI; LIPOPROTEINS; METHIONINE; MICE; PHENOTYPE; SEQUENCE ALIGNMENT; SEQUENCE DELETION; STREPTOCOCCUS PNEUMONIAE; VIRULENCE;

BACTERIA (MICROORGANISMS); MUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84872769080     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049638     Document Type: Article

References (47)

1. Lau GW, Haataja S, Lonetto M, Kensit SE, Marra A, et al. (2001) A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40: 555-571.
2. Darwin AJ, (2005) Genome-wide screens to identify genes of human pathogenic Yersinia species that are expressed during host infection. Curr Issues Mol Biol 7: 135-149.
3. Mei JM, Nourbakhsh F, Ford CW, Holden DW, (1997) Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol Microbiol 26: 399-407.
4. Himpsl SD, Lockatell CV, Hebel JR, Johnson DE, Mobley HL, (2008) Identification of virulence determinants in uropathogenic Proteus mirabilis using signature-tagged mutagenesis. J Med Microbiol 57: 1068-1078.
5. Brown JS, Gilliland SM, Holden DW, (2001) A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol Microbiol 40: 572-585.
6. Brown JS, Gilliland SM, Ruiz-Albert J, Holden DW, (2002) Characterization of pit, a Streptococcus pneumoniae iron uptake ABC transporter. Infect Immun 70: 4389-4398.
7. Basavanna S, Khandavilli S, Yuste J, Cohen JM, Hosie AH, et al. (2009) Screening of Streptococcus pneumoniae ABC transporter mutants demonstrates that LivJHMGF, a branched-chain amino acid ABC transporter, is necessary for disease pathogenesis. Infect Immun 77: 3412-3423.
8. Shelver D, Rajagopal L, Harris TO, Rubens CE, (2003) MtaR, a regulator of methionine transport, is critical for survival of group B streptococcus in vivo. J Bacteriol 185: 6592-6599.
9. Fontecave M, Atta M, Mulliez E, (2004) S-adenosylmethionine: nothing goes to waste. Trends Biochem Sci 29: 243-249.
10. Hullo MF, Auger S, Dassa E, Danchin A, Martin-Verstraete I, (2004) The metNPQ operon of Bacillus subtilis encodes an ABC permease transporting methionine sulfoxide, D- and L-methionine. Res Microbiol 155: 80-86.
11. Merlin C, Gardiner G, Durand S, Masters M, (2002) The Escherichia coli metD locus encodes an ABC transporter which includes Abc (MetN), YaeE (MetI), and YaeC (MetQ). J Bacteriol 184: 5513-5517.
12. den Hengst CD, Groeneveld M, Kuipers OP, Kok J, (2006) Identification and functional characterization of the Lactococcus lactis CodY-regulated branched-chain amino acid permease BcaP (CtrA). J Bacteriol 188: 3280-3289.
13. Bryan JD, Liles R, Cvek U, Trutschl M, Shelver D, (2008) Global transcriptional profiling reveals Streptococcus agalactiae genes controlled by the MtaR transcription factor. BMC Genomics 9: 607.
14. Sperandio B, Gautier C, McGovern S, Ehrlich DS, Renault P, et al. (2007) Control of methionine synthesis and uptake by MetR and homocysteine in Streptococcus mutans. J Bacteriol 189: 7032-7044.
15. Greene RC (1996) Biosynthesis of methionine. In: F.C.Neidhardt, et al., editors. Escherichia coli and Salmonella: cellular and molecular biology: ASM Press, Washington, DC. pp. 542-560.
16. Kovaleva GY, Gelfand MS, (2007) Transcriptional regulation of the methionine and cysteine transport and metabolism in streptococci. FEMS MicrobiolLett 276: 207-215.
17. Ravanel S, Gakiere B, Job D, Douce R, (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95: 7805-7812.
18. Lestrate P, Delrue RM, Danese I, Didembourg C, Taminiau B, et al. (2000) Identification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38: 543-551.
19. Hill CE, Metcalf DS, MacInnes JI, (2003) A search for virulence genes of Haemophilus parasuis using differential display RT-PCR. Vet Microbiol 96: 189-202.
20. Ejim LJ, D'Costa VM, Elowe NH, Loredo-Osti JC, Malo D, et al. (2004) Cystathionine beta-lyase is important for virulence of Salmonella enterica serovar Typhimurium. Infect Immun 72: 3310-3314.
21. Lei B, Liu M, Chesney GL, Musser JM, (2004) Identification of new candidate vaccine antigens made by Streptococcus pyogenes: purification and characterization of 16 putative extracellular lipoproteins. J Infect Dis 189: 79-89.
22. Garmory HS, Titball RW, (2004) ATP-binding cassette transporters are targets for the development of antibacterial vaccines and therapies. Infect Immun 72: 6757-6763.
23. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506.
24. Khandavilli S, Homer KA, Yuste J, Basavanna S, Mitchell T, et al. (2008) Maturation of Streptococcus pneumoniae lipoproteins by a type II signal peptidase is required for ABC transporter function and full virulence. Mol Microbiol 67: 541-557.
25. Severi E, Randle G, Kivlin P, Whitfield K, Young R, et al. (2005) Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter. Mol Microbiol 58: 1173-1185.
26. Thomas GH, Southworth T, Leon-Kempis MR, Leech A, Kelly DJ, (2006) Novel ligands for the extracellular solute receptors of two bacterial TRAP transporters. Microbiology 152: 187-198.
27. Webb AJ, Homer KA, Hosie AH, (2008) Two closely related ABC transporters in Streptococcus mutans are involved in disaccharide and/or oligosaccharide uptake. J Bacteriol 190: 168-178.
28. Brown JS, Ogunniyi AD, Woodrow MC, Holden DW, Paton JC, (2001) Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection. Infect Immun 69: 6702-6706.
29. Johnston JW, Myers LE, Ochs MM, Benjamin WH Jr, Briles DE, et al. (2004) Lipoprotein PsaA in virulence of Streptococcus pneumoniae: surface accessibility and role in protection from superoxide. Infect Immun 72: 5858-5867.
30. Jomaa M, Terry S, Hale C, Jones C, Dougan G, et al. (2006) Immunization with the iron uptake ABC transporter proteins PiaA and PiuA prevents respiratory infection with Streptococcus pneumoniae. Vaccine 24: 5133-5139.
31. Jomaa M, Yuste J, Paton JC, Jones C, Dougan G, et al. (2005) Antibodies to the iron uptake ABC transporter lipoproteins PiaA and PiuA promote opsonophagocytosis of Streptococcus pneumoniae. Infect Immun 73: 6852-6859.
32. Chu J, Shoeman R, Hart J, Coleman T, Mazaitis A, et al. (1985) Cloning and expression of the metE gene in Escherichia coli. Archives of biochemistry and biophysics 239: 467-474.
33. Bayle L, Chimalapati S, Schoehn G, Brown J, Vernet T, et al. (2011) Zinc uptake by Streptococcus pneumoniae depends on both AdcA and AdcAII and is essential for normal bacterial morphology and virulence. Mol Microbiol 82: 904-916.
34. Shah P, Swiatlo E, (2006) Immunization with polyamine transport protein PotD protects mice against systemic infection with Streptococcus pneumoniae. Infect Immun 74: 5888-5892.
35. Shah P, Briles DE, King J, Hale Y, Swiatlo E, (2009) Mucosal immunization with polyamine transport protein D (PotD) protects mice against nasopharyngeal colonization with Streptococcus pneumoniae. Exp Biol Med (Maywood) 234: 403-409.
36. Arevalo MT, Xu Q, Paton JC, Hollingshead SK, Pichichero ME, et al. (2009) Mucosal vaccination with a multicomponent adenovirus-vectored vaccine protects against Streptococcus pneumoniae infection in the lung. FEMS Immunol Med Microbiol 55: 346-351.
37. Novak R, Cauwels A, Charpentier E, Tuomanen E, (1999) Identification of a Streptococcus pneumoniae gene locus encoding proteins of an ABC phosphate transporter and a two-component regulatory system. J Bacteriol 181: 1126-1133.
38. Yuste J, Khandavilli S, Ansari N, Muttardi K, Ismail L, et al. (2010) The effects of PspC on complement-mediated immunity to Streptococcus pneumoniae vary with strain background and capsular serotype. Infect Immu 78: 283-292.
39. Tomasz A (1964) Studies on the competence (for genetic transformation) of Diplococcus pneumoniae in a synthetic medium, abstr G87. Abstr 64th Gen Meet Am Soc Microbiol American Society for Microbiology. Washington, DC.
40. Ogunniyi AD, Giammarinaro P, Paton JC, (2002) The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo. Microbiol 148: 2045-2053.
41. Ogunniyi AD, Mahdi LK, Trappetti C, Verhoeven N, Mermans D, et al. (2012) Identification of genes that contribute to the pathogenesis of invasive pneumococcal disease by in vivo transcriptomic analysis. Infect Immun 80: 3268-3278.
42. Sambrook J EFF, and Maniatis T (1989) Molecular cloning: a laboratory cloning, 2nd ed. New York: Cold Spring Harbor Laboratory Press.
43. Shevchuk NA, Bryksin AV, Nusinovich YA, Cabello FC, Sutherland M, et al. (2004) Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res 32: e19.
44. Maqbool A, Levdikov VM, Blagova EV, Herve M, Horler RS, et al. (2011) Compensating stereochemical changes allow murein tripeptide to be accommodated in a conventional peptide-binding protein. J Biol Chem 286: 31512-31521.
45. Saier MH Jr, (2000) A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol Mol Biol Rev 64: 354-411.
46. Yuste J, Ali S, Sriskandan S, Hyams C, Botto M, et al. (2006) Roles of the alternative complement pathway and C1q during innate immunity to Streptococcus pyogenes. J Immunol 176: 6112-6120.
47. Beuzon CR, Holden DW, (2001) Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect 3: 1345-1352.