Regulation of polysaccharide utilization contributes to the persistence of group A Streptococcus in the oropharynx

Infection and Immunity

Volumn 75, Issue 6, 2007, Pages 2981-2990

  Shelburne III, Samuel A ^a   Okorafor, Nnaja ^a   Sitkiewicz, Izabela ^b   Sumby, Paul ^b   Keith, David ^a   Patel, Payal ^b   Austin, Celest ^a   Graviss, Edward A ^a   Musser, James M ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM MUTANT; COLONY FORMING UNIT; CONTROLLED STUDY; CULTURE MEDIUM; EXPERIMENTAL INFECTION; GENE EXPRESSION; MOUSE; NONHUMAN; NUTRIENT; OROPHARYNX; PHARYNGITIS; PRIORITY JOURNAL; SEROTYPE; STREPTOCOCCUS GROUP A; STREPTOCOCCUS INFECTION;

CARRIER PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; OROPHARYNX; POLYSACCHARIDES; PROTEINS; RNA, BACTERIAL; SALIVA; STREPTOCOCCUS PYOGENES;

EID: 34249912366     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00081-07     Document Type: Article

References (46)

1. Andes, D., A. Lepak, A. Pitula, K. Marchillo, and J. Clark. 2005. A simple approach for estimating gene expression in Candida albicans directly from a systemic infection site. J. Infect. Dis. 192:893-900.
2. Banks, D. J., S. F. Porcella, K. D. Barbian, S. B. Beres, L. E. Philips, J. M. Voyich, F. R. DeLeo, J. M. Martin, G. A. Somerville, and J. M. Musser. 2004. Progress toward characterization of the group A Streptococcus metagenome: complete genome sequence of a macrolide-resistant serotype M6 strain. J. Infect. Dis. 190:727-738.
3. Barrangou, R., M. A. Azcarate-Peril, T. Duong, S. B. Conners, R. M. Kelly, and T. R. Klaenhammer. 2006. Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc. Natl. Acad. Sci. USA 103:3816-3821.
4. Beres, S. B., E. W. Richter, M. J. Nagiec, P. Sumby, S. F. Porcella, F. R. DeLeo, and J. M. Musser. 2006. Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus. Proc. Natl. Acad. Sci. USA 103:7059-7064.
5. Beres, S. B., G. L. Sylva, K. D. Barbian, B. Lei, J. S. Hoff, N. D. Mammarella, M. Y. Liu, J. C. Smoot, S. F. Porcella, L. D. Parkins, D. S. Campbell, T. M. Smith, J. K. McCormick, D. Y. Leung, P. M. Schlievert, and J. M. Musser. 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc. Natl. Acad. Sci. USA 99:10078-10083.
6. Bessen, D. E., A. Manoharan, F. Luo, J. E. Wertz, and D. A. Robinson. 2005. Evolution of transcription regulatory genes is linked to niche specialization in the bacterial pathogen Streptococcus pyogenes. J. Bacteriol. 187:4163-4172.
7. Blehert, D. S., R. J. Palmer, Jr., J. B. Xavier, J. S. Almeida, and P. E. Kolenbrander. 2003. Autoinducer 2 production by Streptococcus gordonii DL1 and the biofilm phenotype of a luxS mutant are influenced by nutritional conditions. J. Bacteriol. 185:4851-4860.
8. Chaussee, M. S., R. O. Watson, J. C. Smoot, and J. M. Musser. 2001. Identification of Rgg-regulated exoproteins of Streptococcus pyogenes. Infect. Immun. 69:822-831.
9. Courtney, H. S., and D. L. Hasty. 1991. Aggregation of group A streptococci by human saliva and effect of saliva on streptococcal adherence to host cells. Infect. Immun. 59:1661-1666.
10. Cunningham, M. W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13:470-511.
11. Dalton, T. L., and J. R. Scott. 2004. CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J. Bacteriol. 186:3928-3937.
12. Egeter, O., and R. Bruckner. 1995. Characterization of a genetic locus essential for maltose-maltotriose utilization in Staphylococcus xylosus. J. Bacteriol. 177:2408-2415.
13. Ferretti, J. J., W. M. McShan, D. Ajdic, D. J. Savic, G. Savic, K. Lyon, C. Primeaux, S. Sezate, A. N. Suvorov, S. Kenton, H. S. Lai, S. P. Lin, Y. Qian, H. G. Jia, F. Z. Najar, Q. Ren, H. Zhu, L. Song, J. White, X. Yuan, S. W. Clifton, B. A. Roe, and R. McLaughlin. 2001. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA 98:4658-4663.
14. Graham, M. R., K. Virtaneva, S. F. Porcella, W. T. Barry, B. B. Gowen, C. R. Johnson, F. A. Wright, and J. M. Musser. 2005. Group A Streptococcus transcriptome dynamics during growth in human blood reveals bacterial adaptive and survival strategies. Am. J. Pathol. 166:455-465.
15. Graham, M. R., K. Virtaneva, S. F. Porcella, D. J. Gardner, R. D. Long, D. M. Welty, W. T. Barry, C. A. Johnson, L. D. Parkins, F. A. Wright, and J. M. Musser. 2006. Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am. J. Pathol. 169:927-942.
16. Green, N. M., S. Zhang, S. F. Porcella, M. J. Nagiec, K. D. Barbian, S. B. Beres, R. B. Lefebvre, and J. M. Musser. 2005. Genome sequence of a serotype M28 strain of group A Streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J. Infect. Dis. 192:760-770.
17. Haralalka, S., S. Nandi, and R. K. Bhadra. 2003. Mutation in the relA gene of Vibrio cholerae affects in vitro and in vivo expression of virulence factors. J. Bacteriol. 185:4672-4682.
18. Holland, I. B., and M. A. Blight. 1999. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293:381-399.
19. Hufnagel, M., S. Koch, R. Creti, L. Baldassarri, and J. Huebner. 2004. A putative sugar-binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J. Infect. Dis. 189:420-430.
20. Hytonen, J., S. Haataja, and J. Finne. 2003. Streptococcus pyogenes glycoprotein-binding strepadhesin activity is mediated by a surface-associated carbohydrate-degrading enzyme, pullulanase. Infect. Immun. 71:784-793.
21. Kreikemeyer, B., K. S. McIver, and A. Podbielski. 2003. Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol. 11:224-232.
22. Kunst, F., N. Ogasawara, I. Moszer, A. M. Albertini, G. Alloni, V. Azevedo, M. G. Bertero, P. Bessieres, A. Bolotin, S. Borchert, R. Borriss, L. Boursier, A. Brans, M. Braun, S. C. Brignell, S. Bron, S. Brouillet, C. V. Bruschi, B. Caldwell, V. Capuano, N. M. Carter, S. K. Choi, J. J. Codani, I. F. Connerton, A. Danchin, et al. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249-256.
23. Kuwayama, H., S. Obara, T. Morio, M. Katoh, H. Urushihara, and Y. Tanaka. 2002. PCR-mediated generation of a gene disruption construct without the use of DNA ligase and plasmid vectors. Nucleic Acids Res. 30:E2.
24. Lukomski, S., N. P. Hoe, I. Abdi, J. Rurangirwa, P. Kordari, M. Liu, S. J. Dou, G. G. Adams, and J. M. Musser. 2000. Nonpolar inactivation of the hypervariable streptococcal inhibitor of complement gene (sic) in serotype M1 Streptococcus pyogenes significantly decreases mouse mucosal colonization. Infect. Immun. 68:535-542.
25. Malke, H., K. Steiner, W. M. McShan, and J. J. Ferretti. 2006. Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA. Int. J. Med. Microbiol.
26. Nakagawa, I., K. Kurokawa, A. Yamashita, M. Nakata, Y. Tomiyasu, N. Okahashi, S. Kawabata, K. Yamazaki, T. Shiba, T. Yasunaga, H. Hayashi, M. Hattori, and S. Hamada. 2003. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res. 13:1042-1055.
27. Nieto, C., M. Espinosa, and A. Puyet. 1997. The maltose/maltodextrin regulon of Streptococcus pneumoniae. Differential promoter regulation by the transcriptional repressor MalR. J. Biol. Chem. 272:30860-30865.
28. Orihuela, C. J., J. N. Radin, J. E. Sublett, G. Gao, D. Kaushal, and E. I. Tuomanen. 2004. Microarray analysis of pneumococcal gene expression during invasive disease. Infect. Immun. 72:5582-5596.
29. Peter, G., and A. L. Smith. 1977. Group A streptococcal infections of the skin and pharynx (second of two parts). N. Engl. J. Med. 297:365-370.
30. Reid, S. D., N. M. Green, J. K. Buss, B. Lei, and J. M. Musser. 2001. Multilocus analysis of extracellular putative virulence proteins made by group A Streptococcus: population genetics, human serologic response, and gene transcription. Proc. Natl. Acad. Sci. USA 98:7552-7557.
31. Reid, S. D., N. M. Green, G. L. Sylva, J. M. Voyich, E. T. Stenseth, F. R. DeLeo, T. Palzkill, D. E. Low, H. R. Hill, and J. M. Musser. 2002. Postgenomic analysis of four novel antigens of group A Streptococcus: growth phase-dependent gene transcription and human serologic response. J. Bacteriol. 184:6316-6324.
32. Roos, V., G. C. Ulett, M. A. Schembri, and P. Klemm. 2006. The asymptomatic bacteriuria Escherichia coli strain 83972 outcompetes uropathogenic E. coli strains in human urine. Infect. Immun. 74:615-624.
33. Shelburne, S. A., III, C. Granville, M. Tokuyama, I. Sitkiewicz, P. Patel, and J. M. Musser. 2005. Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect. Immun. 73:4723-4731.
34. Shelburne, S. A., III, P. Sumby, I. Sitkiewicz, N. Okorafor, C. Granville, P. Patel, J. Voyich, R. Hull, F. R. Deleo, and J. M. Musser. 2006. Maltodextrin utilization plays a key role in the ability of group A Streptococcus to colonize the oropharynx. Infect. Immun. 74:4605-4614.
35. Shelburne, S. A., III, P. Sumby, I. Sitkiewicz, C. N. Granville, F. R. DeLeo, and J. M. Musser. 2005. Central role of a two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc. Natl. Acad. Sci. USA 102:16037-16042.
36. Smoot, J. C., K. D. Barbian, J. J. Van Compel, L. M. Smoot, M. S. Chaussee, G. L. Sylva, D. E. Sturdevant, S. M. Ricklefs, S. F. Porcella, L. D. Parkins, S. B. Beres, D. S. Campbell, T. M. Smith, Q. Zhang, V. Kapur, J. A. Daly, L. G. Veasy, and J. M. Musser. 2002. Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc. Natl. Acad. Sci. USA 99:4668-4673.
37. Snyder, J. A., B. J. Haugen, E. L. Buckles, C. V. Lockatell, D. E. Johnson, M. S. Donnenberg, R. A. Welch, and H. L. Mobley. 2004. Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect. Immun. 72:6373-6381.
38. Steiner, K., and H. Malke. 2001. relA-Independent amino acid starvation response network of Streptococcus pyogenes. J. Bacteriol. 183:7354-7364.
39. Sumby, P., S. F. Porcella, A. G. Madrigal, K. D. Barbian, K. Virtaneva, S. M. Ricklefs, D. E. Sturdevant, M. R. Graham, J. Vuopio-Varkila, N. P. Hoe, and J. M. Musser. 2005. Evolutionary origin and emergence of a highly successful clone of serotype M1 group A Streptococcus involved multiple horizontal gene transfer events. J. Infect. Dis. 192:771-782.
40. Sumby, P., A. R. Whitney, E. A. Graviss, F. R. DeLeo, and J. M. Musser. 2006. Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2:e5.
41. Tchawa Yimga, M., M. P. Leatham, J. H. Allen, D. C. Laux, T. Conway, and P. S. Cohen. 2006. Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect. Immun. 74:1130-1140.
42. 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.
43. Virtaneva, K., M. R. Graham, S. F. Porcella, N. P. Hoe, H. Su, E. A. Graviss, T. J. Gardner, J. E. Allison, W. J. Lemon, J. R. Bailey, M. J. Parnell, and J. M. Musser. 2003. Group A Streptococcus gene expression in humans and cynomolgus macaques with acute pharyngitis. Infect. Immun. 71:2199-2207.
44. Virtaneva, K., S. F. Porcella, M. R. Graham, R. M. Ireland, C. A. Johnson, S. M. Ricklefs, I. Babar, L. D. Parkins, R. A. Romero, G. J. Corn, D. J. Gardner, J. R. Bailey, M. J. Parnell, and J. M. Musser. 2005. Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc. Natl. Acad. Sci. USA 102:9014-9019.
45. Vise, P. D., K. Kodali, N. Hoe, A. Paszczynski, J. M. Musser, and G. W. Daughdrill. 2003. Stable isotope labeling of a group A Streptococcus virulence factor using a chemically defined growth medium. Protein Expr. Purif. 32:232-238.
46. Xu, Q., M. Dziejman, and J. J. Mekalanos. 2003. Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc. Natl. Acad. Sci. USA 100:1286-1291.