Streptococcus pneumoniae can utilize multiple sources of hyaluronic acid for growth

Infection and Immunity

Volumn 80, Issue 4, 2012, Pages 1390-1398

  Marion, Carolyn ^a,b   Stewart, Jason M ^a   Tazi, Mia F ^a   Burnaugh, Amanda M ^a,b   Linke, Caroline M ^a   Woodiga, Shireen A ^a   King, Samantha J ^a,b  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; HYDROLASE; PHOSPHOENOLPYRUVATE; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE; BACTERIAL PROTEIN; GLYCOSIDASE; HYALURONATE LYASE; PHOSPHOTRANSFERASE; POLYSACCHARIDE LYASE; UNSATURATED GLUCURONYL HYDROLASE;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; CARBON SOURCE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; GENE FUNCTION; GENE REARRANGEMENT; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE; ANIMAL; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOUSE;

ANIMALS; BACTERIAL PROTEINS; GLYCOSIDE HYDROLASES; HUMANS; HYALURONIC ACID; MICE; PHOSPHOTRANSFERASES; POLYSACCHARIDE-LYASES; STREPTOCOCCUS PNEUMONIAE;

EID: 84860795291     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05756-11     Document Type: Article

References (47)

1. Abranches J, Chen YY, Burne RA. 2003. Characterization of Streptococcus mutans strains deficient in EIIAB Man of the sugar phosphotransferase system. Appl. Environ. Microbiol. 69:4760-4769.
2. Ashbaugh CD, et al. 2000. Bacterial determinants of persistent throat colonization and the associated immune response in a primate model of human group A streptococcal pharyngeal infection. Cell Microbiol. 2:283-292.
3. Auzat I, et al. 1999. The NADH oxidase of Streptococcus pneumoniae: its involvement in competence and virulence. Mol. Microbiol. 34:1018- 1028.
4. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
5. Berry AM, et al. 1994. Cloning and nucleotide sequence of the Streptococcus pneumoniae hyaluronidase gene and purification of the enzyme from recombinant Escherichia coli. Infect. Immun. 62:1101-1118.
6. Boulnois GJ, et al. 1991. Analysis of some putative protein virulence factors of Streptococcus pneumoniae, p 83-87. In Dunny GM, Cleary PP, Mckay LL (ed), Genetics and molecular biology of streptococci, lactococci, and enterococci. American Society for Microbiology, Washington, DC.
7. Burnaugh AM, Frantz LJ, King SJ. 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J. Bacteriol. 190:221-230.
8. Chapuy-Regaud S, et al. 2003. RegR, a global LacI/GalR family regulator, modulates virulence and competence in Streptococcus pneumoniae. Infect. Immun. 71:2615-2625.
9. Costagliola C, et al. 1996. The ability of bacteria to use Na-hyaluronate as a nutrient. Acta Ophthalmol. Scand. 74:566 -568.
10. Deutscher J, Francke C, Postma PW. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70:939 -1031.
11. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971.
12. Farrell AM, Taylor D, Holland KT. 1995. Cloning, nucleotide sequence determination and expression of the Staphylococcus aureus hyaluronate lyase gene. FEMS Microbiol. Lett. 130:81- 85.
13. Giammarinaro P, Paton JC. 2002. Role of RegM, a homologue of the catabolite repressor protein CcpA, in the virulence of Streptococcus pneumoniae. Infect. Immun. 70:5454 -5461.
14. Guiral S, et al. 2006. Construction and evaluation of a chromosomal expression platform (CEP) for ectopic, maltose-driven gene expression in Streptococcus pneumoniae. Microbiology 152:343-349.
15. Homer KA, Grootveld MC, Hawkes J, Naughton DP, Beighton D. 1994. Degradation of hyaluronate by Streptococcus intermedius strain UNS 35. J. Med. Microbiol. 41:414-422.
16. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61- 68.
17. Husmann LK, Yung DL, Hollingshead SK, Scott JR. 1997. Role of putative virulence factors of Streptococcus pyogenes in mouse models of long-term throat colonization and pneumonia. Infect. Immun. 65:1422- 1430.
18. Iyer R, Camilli A. 2007. Sucrose metabolism contributes to in vivo fitness of Streptococcus pneumoniae. Mol. Microbiol. 66:1-13.
19. Kloosterman TG, Bijlsma JJ, Kok J, Kuipers OP. 2006. To have neighbour's fare: extending the molecular toolbox for Streptococcus pneumoniae. Microbiology 152:351-359.
20. Kornberg HL, Reeves RE. 1972. Inducible phosphoenolpyruvatedependent hexose phosphotransferase activities in Escherichia coli. Biochem. J. 128:1339 -1344.
21. Kostyukova NN, Volkova MO, Ivanova VV, Kvetnaya AS. 1995. A study of pathogenic factors of Streptococcus pneumoniae strains causing meningitis. FEMS Immunol. Med. Microbiol. 10:133-137.
22. Krause RM. 1972. The streptococcal cell: relationship of structure to function and pathogenesis, p 3-18. In Wannamaker LW and Matsen JM (ed), Streptococci and streptoccoccal diseases. Academic Press, Inc., New York, NY.
23. Lacks S, Hotchkiss RD. 1960. A study of the genetic material determining an enzyme in pneumococcus. Biochim. Biophys. Acta 39:508 -518.
24. LeBlanc DJ, Crow VL, Lee LN, Garon CF. 1979. Influence of the lactose plasmid on the metabolism of galactose by Streptococcus lactis. J. Bacteriol. 137:878-884.
25. Marion C, Aten AE, Woodiga SA, King SJ. 2011. Identification of an ATPase, MsmK, which energizes multiple carbohydrate ABC transporters in Streptococcus pneumoniae. Infect. Immun. 79:4193- 4200.
26. Marion C, Burnaugh AM, Woodiga SA, King SJ. 2011. Sialic acid transport contributes to pneumococcal colonization. Infect. Immun. 79: 1262-1269.
27. Marion C, et al. 2009. Identification of a pneumococcal glycosidase that modifies O-linked glycans. Infect. Immun. 77:1389 -1396.
28. Maruyama Y, et al. 2009. Substrate specificity of streptococcal unsaturated glucuronyl hydrolases for sulfated glycosaminoglycan. J. Biol. Chem. 284:18059 -18069.
29. McCool TL, Cate TR, Moy G, Weiser JN. 2002. The immune response to pneumococcal proteins during experimental human carriage. J. Exp. Med. 195:359 -365.
30. McCool TL, Weiser JN. 2004. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect. Immun. 72:5807-5813.
31. McKessar SJ, Hakenbeck R. 2007. The two-component regulatory system TCS08 is involved in cellobiose metabolism of Streptococcus pneumoniae R6. J. Bacteriol. 189:1342-1350.
32. Meng JP, et al. 2008. Identification of Streptococcus pneumoniae genes specifically induced in mouse lung tissues. Can. J. Microbiol. 54:58-65.
33. Monzon ME, Casalino-Matsuda SM, Forteza RM. 2006. Identification of glycosaminoglycans in human airway secretions. Am. J. Respir. Cell Mol. Biol. 34:135-141.
34. Muller-Graf CD, et al. 1999. Population biology of Streptococcus pneumoniae isolated from oropharyngeal carriage and invasive disease. Microbiology 145(Pt 11):3283-3293.
35. Philips BJ, Meguer JX, Redman J, Baker EH. 2003. Factors determining the appearance of glucose in upper and lower respiratory tract secretions. Intensive Care Med. 29:2204 -2210.
36. Rapport MM, Linker A, Meyer K. 1951. The hydrolysis of hyaluronic acid by pneumococcal hyaluronidase. J. Biol. Chem. 192:283-291.
37. Shakhnovich EA, King SJ, Weiser JN. 2002. Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect. Immun. 70:7161-7164.
38. Smith RF, Willett NP. 1968. Rapid plate method for screening hyaluronidase and chondroitin sulfatase-producing microorganisms. Appl. Microbiol. 16:1434 -1436.
39. Starr CR, Engleberg NC. 2006. Role of hyaluronidase in subcutaneous spread and growth of group A streptococcus. Infect. Immun. 74:40-48.
40. Sung CK, Li H, Claverys JP, Morrison DA. 2001. An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl. Environ. Microbiol. 67:5190 -5196.
41. Takao A. 2003. Cloning and expression of hyaluronate lyase genes of Streptococcus intermedius and Streptococcus constellatus subsp. Constellatus (1). FEMS Microbiol. Lett. 219:143-150.
42. Tyx RE, Roche-Hakansson H, Hakansson AP. 2011. Role of dihydrolipoamide dehydrogenase in regulation of raffinose transport in Streptococcus pneumoniae. J. Bacteriol. 193:3512-3524.
43. Wessels MR, Bronze MS. 1994. Critical role of the group A streptococcal capsule in pharyngeal colonization and infection in mice. Proc. Natl. Acad. Sci. U. S. A. 91:12238 -12242.
44. Whatmore AM, Barcus VA, Dowson CG. 1999. Genetic diversity of the streptococcal competence (com) gene locus. J. Bacteriol. 181:3144 -3154.
45. World Health Organization. 2003. Pneumococcal vaccines. Wkly. Epidemiol. Rec. 78:110 -119.
46. Zuniga M, et al. 2005. Horizontal gene transfer in the molecular evolution of mannose PTS transporters. Mol. Biol. Evol. 22:1673-1685.
47. Zwijnenburg PJ, et al. 2001. Experimental pneumococcal meningitis in mice: a model of intranasal infection. J. Infect. Dis. 183:1143-1146.