Naturally occurring single amino acid replacements in a regulatory protein alter streptococcal gene expression and virulence in mice

Journal of Clinical Investigation

Volumn 121, Issue 5, 2011, Pages 1956-1968

  Carroll, Ronan K ^a,d   Shelburne III, Samuel A ^b   Olsen, Randall J ^a   Suber, Bryce ^b   Sahasrabhojane, Pranoti ^b   Kumaraswami, Muthiah ^b   Beres, Stephen B ^a   Shea, Patrick R ^a   Flores, Anthony R ^c   Musser, James M ^a  

^a HOUSTON METHODIST HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d ST JAMES S HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ROPB; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC POLYMORPHISM; HOST PATHOGEN INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS INFECTION;

ALLELES; AMINO ACIDS; ANIMALS; BACTERIAL PROTEINS; DNA; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; KINETICS; MICE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN CONFORMATION; STREPTOCOCCUS; VIRULENCE; VIRULENCE FACTORS;

EID: 79955485771     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45169     Document Type: Article

References (73)

1. Davies HD, et al. Invasive group A streptococcal infections in Ontario, Canada. Ontario Group A Streptococcal Study Group. N Engl J Med. 1996;335(8):547-554. (Pubitemid 26272309)
2. Fridkin SK, et al. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med. 2005;352(14):1436-1444.
3. Laupland KB, Gregson DB, Church DL, Ross T, Pitout JD. Incidence, risk factors and outcomes of Escherichia coli bloodstream infections in a large Canadian region. Clin Microbiol Infect. 2008;14(11):1041-1047. (Pubitemid 352748845)
4. Bae IG, et al. Presence of genes encoding the Panton- Valentine leukocidin exotoxin is not the primary determinant of outcome in patients with complicat ed skin and skin structure infections due to methicillin- resistant Staphylococcus aureus: results of a multinational trial. J Clin Microbiol. 2009;47(12):3952-3957.
5. Afset JE, et al. Identification of virulence genes linked with diarrhea due to atypical enteropathogenic Escherichia coli by DNA microarray analysis and PCR. J Clin Microbiol. 2006;44(10):3703-3711. (Pubitemid 46768784)
6. Lintges M, et al. Superantigen genes are more important than the emm type for the invasiveness of group A Streptococcus infection. J Infect Dis. 2010;202(1):20-28.
7. Fierer J, Guiney DG. Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J Clin Invest. 2001;107(7):775-780. (Pubitemid 32274025)
8. Pirnay JP, et al. Pseudomonas aeruginosa population structure revisited. PLoS One. 2009;4(11):e7740.
9. Lalani T, et al. Associations between the genotypes of Staphylococcus aureus bloodstream isolates and clinical characteristics and outcomes of bacteremic patients. J Clin Microbiol. 2008;46(9):2890-2896.
10. Weinberger DM, et al. Association of serotype with risk of death due to pneumococcal pneumonia: a meta-analysis. Clin Infect Dis. 2010;51(6):692-699.
11. Harris SR, et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science. 2010;327(5964):469-474.
12. He M, et al. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci U S A. 2010;107(16):7527-7532.
13. Beres SB, et al. Molecular complexity of successive bacterial epidemics deconvoluted by comparative pathogenomics. Proc Natl Acad Sci U S A. 2010;107(9):4371-4376.
14. Olsen RJ, et al. Decreased necrotizing fasciitis capacity caused by a single nucleotide mutation that alters a multiple gene virulence axis. Proc Natl Acad Sci U S A. 2010;107(2):888-893.
15. Kennedy AD, et al. Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci U S A. 2008;105(4):1327-1332. (Pubitemid 351397052)
16. Chen SL, et al. Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. Proc Natl Acad Sci U S A. 2009;106(52):22439-22444.
17. Musser JM, Shelburne SA 3rd. A decade of molecular pathogenomic analysis of group A Streptococcus. J Clin Invest. 2009;119(9):2455-2463.
18. Olsen RJ, Shelburne SA, Musser JM. Molecular mechanisms underlying group A streptococcal pathogenesis. Cell Microbiol. 2009;11(1):1-12.
19. McIver KS. Stand-alone response regulators controlling global virulence networks in Streptococcus pyogenes. Contrib Microbiol. 2009;16:103-119.
20. Cho BK, et al. The transcription unit architecture of the Escherichia coli genome. Nat Biotechnol. 2009;27(11):1043-1049.
21. Brown RN, Gulig PA. Roles of RseB, sigmaE, and DegP in virulence and phase variation of colony morphotype of Vibrio vulnificus. Infect Immun. 2009; 77(9):3768-3781.
22. Kreikemeyer B, McIver KS, Podbielski A. Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol. 2003;11(5):224-232. (Pubitemid 36645006)
23. Shelburne SA, et al. A combination of independent transcriptional regulators shapes bacterial virulence gene expression during infection. PLoS Pathog. 2010; 6(3):e1000817.
24. Lyon WR, Gibson CM, Caparon MG. A role for trigger factor and an Rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. EMBO J. 1998; 17(21):6263-6275. (Pubitemid 28497799)
25. Hollands A, Aziz RK, Kansal R, Kotb M, Nizet V, Walker MJ. A naturally occurring mutation in ropB suppresses SpeB expression and reduces M1T1 group A streptococcal systemic virulence. PLoS ONE. 2008;3(12):e4102.
26. Lukomski S, et al. Inactivation of Streptococcus pyogenes extracellular cysteine protease significantly decreases mouse lethality of serotype M3 and M49 strains. J Clin Invest. 1997;99(11):2574-2580. (Pubitemid 27259803)
27. Dmitriev AV, McDowell EJ, Kappeler KV, Chaussee MA, Rieck LD, Chaussee MS. The Rgg regulator of Streptococcus pyogenes influences utilization of non-glucose carbohydrates, prophage induction, and expression of the NAD-glycohydrolase virulence operon. J Bacteriol. 2006;188(20):7230-7241. (Pubitemid 44547628)
28. Chaussee MA, Callegari EA, Chaussee MS. Rgg regulates growth phase-dependent expression of proteins associated with secondary metabolism and stress in Streptococcus pyogenes. J Bacteriol. 2004;186(21):7091-7099. (Pubitemid 39383093)
29. Chaussee MS, Somerville GA, Reitzer L, Musser JM. Rgg coordinates virulence factor synthesis and metabolism in Streptococcus pyogenes. J Bacteriol. 2003;185(20):6016-6024. (Pubitemid 37248453)
30. Loughman JA, Caparon MG. Contribution of invariant residues to the function of Rgg family transcription regulators. J Bacteriol. 2007;189(2):650-655. (Pubitemid 46106398)
31. Kappeler KV, Anbalagan S, Dmitriev AV, McDowell EJ, Neely MN, Chaussee MS. A naturally occurring Rgg variant in serotype M3 Streptococcus pyogenes does not activate speB expression due to altered specificity of DNA binding. Infect Immun. 2009;77(12):5411-5417.
32. Ikebe T, et al. Highly frequent mutations in negative regulators of multiple virulence genes in group A streptococcal toxic shock syndrome isolates. PLoS Pathog. 2010;6(4):e1000832.
33. Declerck N, et al. Structure of PlcR: Insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc Natl Acad Sci U S A. 2007;104(47):18490-18495. (Pubitemid 350210724)
34. Neely MN, Lyon WR, Runft DL, Caparon M. Role of RopB in growth phase expression of the SpeB cysteine protease of Streptococcus pyogenes. J Bacteriol. 2003; 185(17):5166-5174. (Pubitemid 37021978)
35. Loughman JA, Caparon M. Regulation of SpeB in Streptococcus pyogenes by pH and NaCl: a model for in vivo gene expression. J Bacteriol. 2006;188(2):399-408. (Pubitemid 43100527)
36. Musser JM, Stockbauer K, Kapur V, Rudgers GW. Substitution of cysteine 192 in a highly conserved Streptococcus pyogenes extracellular cysteine protease (interleukin 1beta convertase) alters proteolytic activity and ablates zymogen processing. Infect Immun. 1996;64(6):1913-1917. (Pubitemid 26165646)
37. Dmitriev AV, McDowell EJ, Chaussee MS. Inter- and intraserotypic variation in the Streptococcus pyogenes Rgg regulon. FEMS Microbiol Lett. 2008;284(1):43-51. (Pubitemid 351776890)
38. Chaussee MS, Watson RO, Smoot JC, Musser JM. Identification of Rgg-regulated exoproteins of Streptococcus pyogenes. Infect Immun. 2001;69(2):822-831. (Pubitemid 32109545)
39. Wang CH, et al. Effects of oligopeptide permease in group A streptococcal infection. Infect Immun. 2005;73(5):2881-2890.
40. Unnikrishnan M, et al. The bacterial superantigen streptococcal mitogenic exotoxin Z is the major immunoactive agent of Streptococcus pyogenes. J Immunol. 2002;169(5):2561-2569. (Pubitemid 34921001)
41. Zähner D, Scott JR. SipA is required for pilus formation in Streptococcus pyogenes serotype M3. J Bacteriol. 2008;190(2):527-535. (Pubitemid 351360068)
42. Banks DJ, Lei B, Musser JM. Prophage induction and expression of prophage-encoded virulence factors in group A Streptococcus serotype M3 strain MGAS315. Infect Immun. 2003;71(12):7079-7086. (Pubitemid 37475340)
43. Gase K, Ferretti JJ, Primeaux C, McShan WM. Identification, cloning, and expression of the CAMP factor gene (cfa) of group A streptococci. Infect Immun. 1999;67(9):4725-4731. (Pubitemid 29400456)
44. Ribardo DA, McIver KS. Defining the Mga regulon: Comparative transcriptome analysis reveals both direct and indirect regulation by Mga in the group A Streptococcus. Mol Microbiol. 2006;62(2):491-508. (Pubitemid 44477237)
45. Shelburne SA 3rd, et al. A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc Natl Acad Sci U S A. 2008;105(5):1698-1703.
46. Voyich JM, et al. Engagement of the pathogen survival response used by group A Streptococcus to avert destruction by innate host defense. J Immunol. 2004; 173(2):1194-1201. (Pubitemid 38924296)
47. Chaussee MS, et al. Rgg influences the expression of multiple regulatory loci to coregulate virulence factor expression in Streptococcus pyogenes. Infect Immun. 2002;70(2):762-770. (Pubitemid 34083838)
48. Nizet V, et al. Genetic locus for streptolysin S production by group A Streptococcus. Infect Immun. 2000; 68(7):4245-4254. (Pubitemid 30434580)
49. Carlsson F, Berggard K, Stalhammar-Carlemalm M, Lindahl G. Evasion of phagocytosis through cooperation between two ligand-binding regions in Streptococcus pyogenes M protein. J Exp Med. 2003; 198(7):1057-1068. (Pubitemid 37248621)
50. Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM. Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2006;2(1):e5.
51. Walker MJ, et al. DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med. 2007;13(8):981-985. (Pubitemid 47222039)
52. Engleberg NC, Heath A, Miller A, Rivera C, DiRita VJ. Spontaneous mutations in the CsrRS two-component regulatory system of Streptococcus pyogenes result in enhanced virulence in a murine model of skin and soft tissue infection. J Infect Dis. 2001; 183(7):1043-1054. (Pubitemid 32230952)
53. Aziz RK, et al. Invasive M1T1 group A Streptococcus undergoes a phase-shift in vivo to prevent proteolytic degradation of multiple virulence factors by SpeB. Mol Microbiol. 2004;51(1):123-134. (Pubitemid 38031076)
54. Kansal RG, Datta V, Aziz RK, Abdeltawab NF, Rowe S, Kotb M. Dissection of the molecular basis for hypervirulence of an in vivo-selected phenotype of the widely disseminated M1T1 strain of group A Streptococcus bacteria. J Infect Dis. 2010;201(6):855-865.
55. Khor CC, et al. CISH and susceptibility to infectious diseases. N Engl J Med. 2010;362(22):2092-2101.
56. Zhang FR, et al. Genomewide association study of leprosy. N Engl J Med. 2009;361(27):2609-2618.
57. Turner CE, Kurupati P, Jones MD, Edwards RJ, Sriskandan S. Emerging role of the interleukin-8 cleaving enzyme SpyCEP in clinical Streptococcus pyogenes infection. J Infect Dis. 2009;200(4):555-563.
58. Smith EE, et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A. 2006;103(22):8487-8492. (Pubitemid 43838482)
59. Zhu Y, Inouye M. The role of the G2 box, a conserved motif in the histidine kinase superfamily, in modulating the function of EnvZ. Mol Microbiol. 2002; 45(3):653-663. (Pubitemid 34989174)
60. Sharkawy A, et al. Severe group A streptococcal soft-tissue infections in Ontario:1992-1996. Clin Infect Dis. 2002;34(4):454-460.
61. Wu S, Skolnick J, Zhang Y. Ab initio modeling of small proteins by iterative TASSER simulations. BMC Biol. 2007;5:17.
62. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9:40.
63. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60(12 pt 1):2126-2132. (Pubitemid 41742764)
64. DeLano WL. The PyMOL Molecular Graphics System. Palo Alto California, USA: DeLano Scientific; 2002.
65. Shelburne SA 3rd, et al. Maltodextrin utilization plays a key role in the ability of group A Streptococcus to colonize the oropharynx. Infect Immun. 2006; 74(8):4605-4614.
66. Kuwayama H, Obara S, Morio T, Katoh M, Urushihara H, Tanaka Y. PCR-mediated generation of a gene disruption construct without the use of DNA ligase and plasmid vectors. Nucleic Acids Res. 2002;30(2):E2.
67. Lukomski S, et al. Nonpolar inactivation of the hypervariable streptococcal inhibitor of complement gene (sic) in serotype M1 Streptococcus pyogenes significantly decreases mouse mucosal colonization. Infect Immun. 2000;68(2):535-542. (Pubitemid 30056504)
68. Li J, Kasper DL, Ausubel FM, Rosner B, Michel JL. Inactivation of the alpha C protein antigen gene, bca, by a novel shuttle/suicide vector results in attenuation of virulence and immunity in group B Streptococcus. Proc Natl Acad Sci U S A. 1997; 94(24):13251-13256. (Pubitemid 27518508)
69. Perez-Casal J, Price JA, Maguin E, Scott JR. An M protein with a single C repeat prevents phagocytosis of Streptococcus pyogenes: use of a temperature-sensitive shuttle vector to deliver homologous sequences to the chromosome of S. pyogenes. Mol Microbiol. 1993;8(5):809-819. (Pubitemid 23171463)
70. Graham MR, et al. Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am J Pathol. 2006;169(3):927-942. (Pubitemid 44418730)
71. Virtaneva K, et al. Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci U S A. 2005;102(25):9014-9019. (Pubitemid 40881070)
72. Lyon WR, Caparon MG. Trigger factor-mediated prolyl isomerization influences maturation of the Streptococcus pyogenes cysteine protease. J Bacteriol. 2003; 185(12):3661-3667. (Pubitemid 36676433)
73. Lei B, Mackie S, Lukomski S, Musser JM. Identification and immunogenicity of group A Streptococcus culture supernatant proteins. Infect Immun. 2000; 68(12):6807-6818. (Pubitemid 32463388)