Surface export of GAPDH/SDH, a glycolytic enzyme, is essential for streptococcus pyogenes virulence

mBio

Volumn 2, Issue 3, 2011, Pages

  Jin, Hong ^a   Agarwal, Shivangi ^a   Agarwal, Shivani ^a   Pancholi, Vijay ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PLASMINOGEN; STREPTOCCAL SURFACE DEHYDROGENASE; STREPTOLYSIN S; UNCLASSIFIED DRUG; AMINO ACID; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP); MEMBRANE PROTEIN; MUTANT PROTEIN; VIRULENCE FACTOR;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE GENE; LIPID METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STREPTOCCAL SURFACE DEHYDROGENASE GENE; STREPTOCOCCUS GROUP A; STREPTOCOCCUS PYOGENES; UPREGULATION; ANIMAL; DISEASE MODEL; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; RODENT DISEASE; STREPTOCOCCUS INFECTION; VIRULENCE;

BACTERIA (MICROORGANISMS); MAMMALIA; PROKARYOTA; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SP. 'GROUP A';

AMINO ACIDS; ANIMALS; CARBOHYDRATE METABOLISM; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE (NADP+); LIPID METABOLISM; MEMBRANE PROTEINS; METABOLIC NETWORKS AND PATHWAYS; MICE; MICROARRAY ANALYSIS; MUTANT PROTEINS; RODENT DISEASES; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; VIRULENCE; VIRULENCE FACTORS;

EID: 84855188274     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00068-11     Document Type: Article

References (55)

1. Tart AH, Walker MJ, Musser JM. 2007. New understanding of the group A Streptococcus pathogenesis cycle. Trends Microbiol. 15:318-325.
2. Carapetis JR, Steer AC, Mulholland EK, Weber M. 2005. The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5:685-694.
3. Kreikemeyer B, McIver KS, Podbielski A. 2003. Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol. 11:224-232.
4. Churchward G. 2007. The two faces of Janus: virulence gene regulation by CovR/S in group A streptococci. Mol. Microbiol. 64:34-41.
5. McIver KS. 2009. Stand-alone response regulators controlling global virulence networks in Streptococcus pyogenes. Contrib. Microbiol. 16: 103-119.
6. Shelburne SA, et al. 2005. Central role of a bacterial two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc. Natl. Acad. Sci. U. S. A. 102:16037-16042.
7. Cho KH, Caparon MG. 2005. Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes. Mol. Microbiol. 57:1545-1556.
8. Virtaneva K, et al. 2005. Longitudinal analysis of the group A Streptococ-cus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc. Natl. Acad. Sci. U. S. A. 102:9014-9019.
9. Almengor AC, Kinkel TL, Day SJ, McIver KS. 2007. The catabolite control protein CcpA binds to Pmga and influences expression of the virulence regulator Mga in the group A Streptococcus. J. Bacteriol. 189: 8405-8416.
10. Shelburne SA, et al. 2008. A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc. Natl. Acad. Sci. U. S. A. 105:1698-1703.
11. Deutscher J. 2008. The mechanisms of carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 11:87-93.
12. Pancholi V, Fischetti VA. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate dehydrogenase with multiple binding activity. J. Exp. Med. 176:415-426.
13. Pancholi V. 2001. Multifunctional alpha-enolase: its role in diseases. Cell. Mol. Life Sci. 58:902-920.
14. Pancholi V, Chhatwal GS. 2003. Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol. 293:1-11.
15. Matta SK, Agarwal S, Bhatnagar R. 2010. Surface localized and extracellular glyceraldehyde-3-phosphate dehydrogenase of Bacillus anthracis is a plasminogen binding protein. Biochim. Biophys. Acta 1804:2111-2120.
16. Pancholi V, Fischetti VA. 1993. Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme. Proc. Natl. Acad. Sci. U. S. A. 90:8154-8158.
17. Lottenberg R, et al. 1992. Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J. Bacteriol. 174: 5204-5210.
18. Boel G, Jin H, Pancholi V. 2005. Inhibition of cell surface export of group A streptococcal anchorless surface dehydrogenase affects bacterial adherence and antiphagocytic properties. Infect. Immun. 73:6237-6248.
19. Jin H, Song YP, Boel G, Kochar J, Pancholi V. 2005. Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. J. Mol. Biol. 350:27-41.
20. Pancholi V, Fischetti VA. 1997. Regulation of the phosphorylation of human pharyngeal cell proteins by group A streptococcal surface dehydrogenase (SDH): signal transduction between streptococci and pharyngeal cells. J. Exp. Med. 186:1633-1643.
21. Alvarez-Dominguez C, et al. 2008. Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic 9:325-337.
22. Terao Y, Yamaguchi M, Hamada S, Kawabata S. 2006. Multifunctional glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pyogenes is essential for evasion from neutrophils. J. Biol. Chem. 281: 14215-14223.
23. Rosinha GM, Myioshi A, Azevedo V, Splitter GA, Oliveira SC. 2002. Molecular and immunological characterisation of recombinant Brucella abortus glyceraldehyde-3-phosphate-dehydrogenase, a T- and B-cell reactive protein that induces partial protection when co-administered with an interleukin-12-expressing plasmid in a DNA vaccine formulation. J. Med. Microbiol. 51:661-671.
24. Liu Y, Oshima S, Kurohara K, Ohnishi K, Kawai K. 2005. Vaccine efficacy of recombinant GAPDH of Edwardsiella tarda against edwardsiellosis. Microbiol. Immunol. 49:605-612.
25. Madureira P, et al. 2007. Streptococcus agalactiae GAPDH is a virulenceassociated immunomodulatory protein. J. Immunol. 178:1379-1387.
26. Ferretti JJ, et al. 2001. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. U. S. A. 98:4658-4663.
27. Shelburne SA, Davenport MT, Keith DB, Musser JM. 2008. The role of complex carbohydrate catabolism in the pathogenesis of invasive streptococci. Trends Microbiol. 16:318-325.
28. Degnan BA, et al. 1998. Inhibition of human peripheral blood mononuclear cell proliferation by Streptococcus pyogenes cell extract is associated with arginine deiminase activity. Infect. Immun. 66:3050-3058.
29. Marouni MJ, Ziomek E, Sela S. 2003. Influence of group A streptococcal acid glycoprotein on expression of major virulence factors and internalization by epithelial cells. Microb. Pathog. 35:63-72.
30. Postma PW, Lengeler JW. 1985. Phosphoenolpyruvate: carbohydrate phosphotransferase system of bacteria. Microbiol. Rev. 49:232-269.
31. Thevenot T, Brochu D, Vadeboncoeur C, Hamilton IR. 1995. Regulation of ATP-dependent P-(Ser)-HPr formation in Streptococcus mutans and Streptococcus salivarius. J. Bacteriol. 177:2751-2759.
32. Schujman GE, de Mendoza D. 2008. Regulation of type II fatty acid synthase in gram-positive bacteria. Curr. Opin. Microbiol. 11:148-152.
33. Datta V, et al. 2005. Mutational analysis of the group A streptococcal operon encoding streptolysin S and its virulence role in invasive infection. Mol. Microbiol. 56:681-695.
34. Chiang-Ni C, Wu JJ. 2008. Effects of streptococcal pyrogenic exotoxin B on pathogenesis of Streptococcus pyogenes. J. Formos. Med. Assoc. 107: 677-685.
35. Shelburne SA, et al. 2010. A combination of independent transcriptional regulators shapes bacterial virulence gene expression during infection. PLoS Pathog. 6:e1000817.
36. Shelburne SA, et al. 2006. Maltodextrin utilization plays a key role in the ability of groupAStreptococcus to colonize the oropharynx. Infect. Immun. 74:4605-4614.
37. Roy DJ, Casabon I, Vaillancourt K, Huot JL, Vadeboncoeur C. 2008. Streptococci and lactococci synthesize large amounts of HPr(Ser-P) (His- P). Can. J. Microbiol. 54:941-949.
38. Takase K, et al. 1994. Sequencing and characterization of the ntp gene cluster for vacuolar-type Na([+)-translocation ATPase of Enterococcus hirae. J. Biol. Chem. 269:11037-11044.
39. Lu YJ, Rock CO. 2006. Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol. Microbiol. 59:551-566.
40. Balemans W, et al. 2010. Essentiality of FASII pathway for Staphylococcus aureus. Nature 463:E3-E5.
41. Fozo EM, Scott-Anne K, Koo H, Quivey RG. 2007. Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect. Immun. 75:1537-1539.
42. Pancholi V, Fontan PA, Jin H. 2003. Plasminogen-mediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells. Microb. Pathog. 35:293-303.
43. Graham MR, et al. 2002. Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc. Natl. Acad. Sci. U. S. A. 99:13855-13860.
44. Ribardo DA, McIver KS. 2009. Defining the Mga regulon: comparative tranascriptome analysis reveals both direct and indirect regulation by Mga in the group A Streptococcus. Mol. Microbiol. 62:491-508.
45. Dmitriev AV, et al. 2006. The Rgg regulator of Streptococcus pyogenes influences utilization of nonglucose carbohydrates, prophage induction, and expression of the NAD-glycohydrolase virulence operon. J. Bacteriol. 188:7230-7241.
46. Rosch J, Caparon M. 2004. A microdomain for protein secretion in gram-positive bacteria. Science 304:1513-1515.
47. Pancholi V, Fischetti VA. 1998. Alpha-enolase, a novel strong plasmin-(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273:14503-14515.
48. van de Rijn I, Kessler RE. 1980. Growth characteristics of group A streptococci in a new chemically defined medium. Infect. Immun. 27: 444-448.
49. Pancholi V, Boël G, Jin H. 2010. Streptococcus pyogenes Ser/Thr kinaseregulated cell wall hydrolase is a cell division plane-recognizing and chainforming virulence factor. J. Biol. Chem. 285:30861-30874.
50. Jin H, Pancholi V. 2006. Identification and biochemical characterization of a eukaryotic-type serine/threonine kinase and its cognate phosphatase in Streptococcus pyogenes: their biological functions and substrate identification. J. Mol. Biol. 357:1351-1372.
51. Jones KF, Fischetti VA. 1987. Biological and immunochemical identity of M protein on group G streptococci with M protein on group A streptococci. Infect. Immun. 55:502-506.
52. Fontán PA, Pancholi V, Nociari MM, Fischetti VA. 2000. Antibodies to streptococcal surface enolase react with human alpha-enolase: implications in poststreptococcal sequelae. J. Infect. Dis. 182:1712-1721.
53. Ravins M, et al. 2000. Characterization of a mouse-passaged, highly encapsulated variant of group A Streptococcus in in vitro and in vivo studies. J. Infect. Dis. 182:1702-1711.
54. Collin M, Olsén A. 2000. Generation of a mature streptococcal cysteine proteinase is dependent on cell wall-anchored M1 protein. Mol. Microbiol. 36:1306-1318.
55. Ma Y, et al. 2006. Identification and characterization of bicistronic speB and prsA gene expression in the group A Streptococcus. J. Bacteriol. 188: 7626-7634.