Natural variation in the promoter of the gene encoding the mga regulator alters host-pathogen interactions in group a streptococcus carrier strains

Infection and Immunity

Volumn 81, Issue 11, 2013, Pages 4128-4138

  Flores, Anthony R ^a,b   Olsen, Randall J ^b   Wunsche, Andrea ^b   Kumaraswami, Muthiah ^b   Shelburne III, Samuel A ^c   Carroll, Ronan K ^b,d   Musser, James M ^b  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

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

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL; REGULATOR PROTEIN; REGULATOR PROTEIN CODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BLOOD CULTURE; CONTROLLED STUDY; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; HUMAN; MGA PROMOTER; MOUSE; NECROTIZING FASCIITIS; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SEROTYPE; STREPTOCOCCUS GROUP A;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CARRIER STATE; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA FASCICULARIS; MICE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; RECOMBINATION, GENETIC; SEQUENCE DELETION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

EID: 84886774349     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00405-13     Document Type: Article

References (62)

1. Yazdankhah SP, Caugant DA. 2004. Neisseria meningitidis: an overview of the carriage state. J. Med. Microbiol. 53:821-832.
2. Bogaert D, van Belkum A, Sluijter M, Luijendijk A, de Groot R, Rumke HC, Verbrugh HA, Hermans PW. 2004. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 363: 1871-1872.
3. Graham PL, III, Lin SX, Larson EL. 2006. A U.S. population-based survey of Staphylococcus aureus colonization. Ann. Intern. Med. 144:318- 325.
4. Cockerill FR, III, MacDonald KL, Thompson RL, Roberson F, Kohner PC, Besser-Wiek J, Manahan JM, Musser JM, Schlievert PM, Talbot J, Frankfort B, Steckelberg JM, Wilson WR, Osterholm MT. 1997. An outbreak of invasive group A streptococcal disease associated with high carriage rates of the invasive clone among school-aged children. JAMA 277:38-43.
5. Crum NF, Russell KL, Kaplan EL, Wallace MR, Wu J, Ashtari P, Morris DJ, Hale BR. 2005. Pneumonia outbreak associated with group A Streptococcus species at a military training facility. Clin. Infect. Dis. 40:511- 518.
6. Engelgau MM, Woernle CH, Schwartz B, Vance NJ, Horan JM. 1994. Invasive group A streptococcus carriage in a child care centre after a fatal case. Arch. Dis. Child. 71:318-322.
7. Haukness HA, Tanz RR, Thomson RB, Jr, Pierry DK, Kaplan EL, Beall B, Johnson D, Hoe NP, Musser JM, Shulman ST. 2002. The heterogeneity of endemic community pediatric group A streptococcal pharyngeal isolates and their relationship to invasive isolates. J. Infect. Dis. 185:915- 920.
8. Jackson LA, Neuzil KM, Yu O, Benson P, Barlow WE, Adams AL, Hanson CA, Mahoney LD, Shay DK, Thompson WW. 2003. Effectiveness of pneumococcal polysaccharide vaccine in older adults. N. Engl. J. Med. 348:1747-1755.
9. Millar EV, Watt JP, Bronsdon MA, Dallas J, Reid R, Santosham M, O'Brien KL. 2008. Indirect effect of 7-valent pneumococcal conjugate vaccine on pneumococcal colonization among unvaccinated household members. Clin. Infect. Dis. 47:989-996.
10. Poehling KA, Talbot TR, Griffin MR, Craig AS, Whitney CG, Zell E, Lexau CA, Thomas AR, Harrison LH, Reingold AL, Hadler JL, Farley MM, Anderson BJ, Schaffner W. 2006. Invasive pneumococcal disease among infants before and after introduction of pneumococcal conjugate vaccine. JAMA 295:1668-1674.
11. Roy S, Kaplan EL, Rodriguez B, Schreiber JR, Salata RA, Palavecino E, John CC. 2003. A family cluster of five cases of group A streptococcal pneumonia. Pediatrics 112:e61- e65. doi:10.1542/peds.112.1.e61.
12. Krause RM, Rammelkamp CH, Jr. 1962. Studies of the carrier state following infection with group A streptococci. II. Infectivity of streptococci isolated during acute pharyngitis and during the carrier state. J. Clin. Invest. 41:575-578.
13. Krause RM, Rammelkamp CH, Jr, Denny FW, Jr, Wannamaker LW. 1962. Studies of the carrier state following infection with group A streptococci. 1. Effect of climate. J. Clin. Invest. 41:568-574.
14. Rothbard S, Watson RF. 1948. Variation occurring in group A streptococci during human infection. Progressive loss of M substance correlated with increasing susceptibility to bacteriostasis. J. Exp. Med. 87:521-533.
15. Johnson DR, Kurlan R, Leckman J, Kaplan EL. 2010. The human immune response to streptococcal extracellular antigens: clinical, diagnostic, and potential pathogenetic implications. Clin. Infect. Dis. 50:481- 490.
16. Martin JM, Green M, Barbadora KA, Wald ER. 2004. Group A streptococci among school-aged children: clinical characteristics and the carrier state. Pediatrics 114:1212-1219.
17. Carapetis JR. 2005. Current evidence for the burden of group A streptococcal diseases. World Health Organization, Geneva, Switzerland.
18. Committee on Infectious Diseases. 2009. Group A streptococcal infections, p 616-628. In Pickering LK (ed), Red book, 28th ed. American Academy of Pediatrics, Elk Grove Village, IL.
19. Shaikh N, Leonard E, Martin JM. 2010. Prevalence of streptococcalpharyngitis and streptococcal carriage in children: a meta-analysis. Pediatrics 126:e557- e564. doi:10.1542/peds.2009-2648.
20. Lancefield RC. 1962. Current knowledge of type-specific M antigens of group A streptococci. J. Immunol. 89:307-313.
21. Lancefield RC. 1959. Persistence of type-specific antibodies in man following infection with group A streptococci. J. Exp. Med. 110:271- 292.
22. Beres SB, Richter EW, Nagiec MJ, Sumby P, Porcella SF, DeLeo FR, Musser JM. 2006. Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus. Proc. Natl. Acad. Sci. U. S. A. 103:7059-7064.
23. Caparon MG, Scott JR. 1987. Identification of a gene that regulates expression of M protein, the major virulence determinant of group A streptococci. Proc. Natl. Acad. Sci. U. S. A. 84:8677-8681.
24. McIver KS, Heath AS, Green BD, Scott JR. 1995. Specific binding of the activator Mga to promoter sequences of the emm and scpA genes in the group A streptococcus. J. Bacteriol. 177:6619-6624.
25. McIver KS, Thurman AS, Scott JR. 1999. Regulation of mga transcription in the group A streptococcus: specific binding of mga within its own promoter and evidence for a negative regulator. J. Bacteriol. 181:5373- 5383.
26. Okada N, Geist RT, Caparon MG. 1993. Positive transcriptional control of mry regulates virulence in the group A streptococcus. Mol. Microbiol. 7:893-903.
27. Hoe NP, Fullerton KE, Liu M, Peters JE, Gackstetter GD, Adams GJ, Musser JM. 2003. Molecular genetic analysis of 675 group A streptococcus isolates collected in a carrier study at Lackland Air Force Base, San Antonio, Texas. J. Infect. Dis. 188:818-827.
28. Musser JM, Hauser AR, Kim MH, Schlievert PM, Nelson K, Selander RK. 1991. Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: clonal diversity and pyrogenic exotoxin expression. Proc. Natl. Acad. Sci. U. S. A. 88:2668-2672.
29. Beres SB, Sylva GL, Barbian KD, Lei B, Hoff JS, Mammarella ND, Liu MY, Smoot JC, Porcella SF, Parkins LD, Campbell DS, Smith TM, McCormick JK, Leung DY, Schlievert PM, Musser JM. 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: phageencoded toxins, the high-virulence phenotype, and clone emergence. Proc. Natl. Acad. Sci. U. S. A. 99:10078-10083.
30. Beres SB, Carroll RK, Shea PR, Sitkiewicz I, Martinez-Gutierrez JC, Low DE, McGeer A, Willey BM, Green K, Tyrrell GJ, Goldman TD, Feldgarden M, Birren BW, Fofanov Y, Boos J, Wheaton WD, Honisch C, Musser JM. 2010. Molecular complexity of successive bacterial epidemics deconvoluted by comparative pathogenomics. Proc. Natl. Acad. Sci. U. S. A. 107:4371-4376.
31. Beres SB, Sylva GL, Sturdevant DE, Granville CN, Liu M, Ricklefs SM, Whitney AR, Parkins LD, Hoe NP, Adams GJ, Low DE, DeLeo FR, McGeer A, Musser JM. 2004. Genome-wide molecular dissection of serotype M3 group A Streptococcus strains causing two epidemics of invasive infections. Proc. Natl. Acad. Sci. U. S. A. 101:11833-11838.
32. Gryllos I, Grifantini R, Colaprico A, Cary ME, Hakansson A, Carey DW, Suarez-Chavez M, Kalish LA, Mitchell PD, White GL, Wessels MR. 2008. PerR confers phagocytic killing resistance and allows pharyngeal colonization by group A Streptococcus. PLoS Pathog. 4:e1000145. doi:10.1371/journal.ppat.1000145.
33. Li J, Kasper DL, Ausubel FM, Rosner B, Michel JL. 1997. 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. 94:13251-13256.
34. Carroll RK, Shelburne SA, III, Olsen RJ, Suber B, Sahasrabhojane P, Kumaraswami M, Beres SB, Shea PR, Flores AR, Musser JM. 2011. Naturally occurring single amino acid replacements in a regulatory protein alter streptococcal gene expression and virulence in mice. J. Clin. Invest. 121:1956-1968.
35. Lukomski S, Hoe NP, Abdi I, Rurangirwa J, Kordari P, Liu M, Dou SJ, Adams GG, Musser JM. 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.
36. Olsen RJ, Sitkiewicz I, Ayeras AA, Gonulal VE, Cantu C, Beres SB, Green NM, Lei B, Humbird T, Greaver J, Chang E, Ragasa WP, Montgomery CA, Cartwright J, Jr, McGeer A, Low DE, Whitney AR, Cagle PT, Blasdel TL, DeLeo FR, Musser JM. 2010. Decreased necrotizingfasciitis capacity caused by a single nucleotide mutation that alters a multiple gene virulence axis. Proc. Natl. Acad. Sci. U. S. A. 107:888-893.
37. Lancefield RC. 1957. Differentiation of group A streptococci with a common R antigen into three serological types, with special reference to the bactericidal test. J. Exp. Med. 106:525-544.
38. Flores AR, Jewell BE, Fittipaldi N, Beres SB, Musser JM. 2012. Human disease isolates of serotype m4 and m22 group a streptococcus lack genes required for hyaluronic acid capsule biosynthesis. mBio 3:e00413-12. doi: 10.1128/mBio.00413-12.
39. Chaussee MS, Watson RO, Smoot JC, Musser JM. 2001. Identification of Rgg-regulated exoproteins of Streptococcus pyogenes. Infect. Immun. 69:822-831.
40. Virtaneva K, Porcella SF, Graham MR, Ireland RM, Johnson CA, Ricklefs SM, Babar I, Parkins LD, Romero RA, Corn GJ, Gardner DJ, Bailey JR, Parnell MJ, Musser JM. 2005. Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc. Natl. Acad. Sci. U. S. A. 102:9014-9019.
41. Lukomski S, Nakashima K, Abdi I, Cipriano VJ, Ireland RM, Reid SD, Adams GG, Musser JM. 2000. Identification and characterization of the scl gene encoding a group A Streptococcus extracellular protein virulence factor with similarity to human collagen. Infect. Immun. 68:6542-6553.
42. Schroeder B, Boyle MD, Sheerin BR, Asbury AC, Lottenberg R. 1999. Species specificity of plasminogen activation and acquisition of surfaceassociated proteolytic activity by group C streptococci grown in plasma. Infect. Immun. 67:6487-6495.
43. Wang H, Lottenberg R, Boyle MD. 1995. Analysis of the interaction of groupAstreptococci with fibrinogen, streptokinase and plasminogen. Microb. Pathog. 18:153-166.
44. McIver KS, Scott JR. 1997. Role of mga in growth phase regulation of virulence genes of the group A streptococcus. J. Bacteriol. 179:5178-5187.
45. Ji Y, McLandsborough L, Kondagunta A, Cleary PP. 1996. C5a peptidase alters clearance and trafficking of group A streptococci by infected mice. Infect. Immun. 64:503-510.
46. Wexler DE, Chenoweth DE, Cleary PP. 1985. Mechanism of action of the group A streptococcal C5a inactivator. Proc. Natl. Acad. Sci. U. S. A. 82:8144-8148.
47. Caswell CC, Lukomska E, Seo NS, Hook M, Lukomski S. 2007. Scl1- dependent internalization of groupAStreptococcus via direct interactions with the alpha2beta(1) integrin enhances pathogen survival and reemergence. Mol. Microbiol. 64:1319-1331.
48. Ashbaugh CD, Moser TJ, Shearer MH, White GL, Kennedy RC, Wessels MR. 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.
49. Stenz L, Francois P, Whiteson K, Wolz C, Linder P, Schrenzel J. 2011. The CodY pleiotropic repressor controls virulence in gram-positive pathogens. FEMS Immunol. Med. Microbiol. 62:123-139.
50. Kreth J, Chen Z, Ferretti J, Malke H. 2011. Counteractive balancing of transcriptome expression involving CodY and CovRS in Streptococcus pyogenes. J. Bacteriol. 193:4153-4165.
51. Malke H, Ferretti JJ. 2007. CodY-affected transcriptional gene expression of Streptococcus pyogenes during growth in human blood. J. Med. Microbiol. 56:707-714.
52. Malke H, Steiner K, McShan WM, Ferretti JJ. 2006. Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA. Int. J. Med. Microbiol. 296:259- 275.
53. Caugant DA, Tzanakaki G, Kriz P. 2007. Lessons from meningococcal carriage studies. FEMS Microbiol. Rev. 31:52-63.
54. Monecke S, Luedicke C, Slickers P, Ehricht R. 2009. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur. J. Clin. Microbiol. Infect. Dis. 28:1159-1165.
55. Schoen C, Blom J, Claus H, Schramm-Gluck A, Brandt P, Muller T, Goesmann A, Joseph B, Konietzny S, Kurzai O, Schmitt C, Friedrich T, Linke B, Vogel U, Frosch M. 2008. Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc. Natl. Acad. Sci. U. S. A. 105:3473-3478.
56. Sivaraman K, Venkataraman N, Tsai J, Dewell S, Cole AM. 2008. Genome sequencing and analysis reveals possible determinants of Staphylococcus aureus nasal carriage. BMC Genomics 9:433. doi:10.1186/1471 -2164-9-433.
57. Ribardo DA, McIver KS. 2006. Defining the Mga regulon: Comparativetranscriptome analysis reveals both direct and indirect regulation by Mga in the group A streptococcus. Mol. Microbiol. 62:491-508.
58. Moxon R, Bayliss C, Hood D. 2006. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet. 40:307-333.
59. Martin P, Makepeace K, Hill SA, Hood DW, Moxon ER. 2005. Microsatellite instability regulates transcription factor binding and gene expression. Proc. Natl. Acad. Sci. U. S. A. 102:3800-3804.
60. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM, Burns JL, Kaul R, Olson MV. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 103:8487-8492.
61. Yang L, Jelsbak L, Marvig RL, Damkiaer S, Workman CT, Rau MH, Hansen SK, Folkesson A, Johansen HK, Ciofu O, Hoiby N, Sommer MO, Molin S. 2011. Evolutionary dynamics of bacteria in a human host environment. Proc. Natl. Acad. Sci. U. S. A. 108:7481-7486.
62. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, Davis MR, Jr, Skurnik D, Leiby N, LiPuma JJ, Goldberg JB, McAdam AJ, Priebe GP, Kishony R. 2011. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat. Genet. 43:1275- 1280.