DrsG from Streptococcus dysgalactiae subsp. equisimilis inhibits the antimicrobial peptide LL-37

Infection and Immunity

Volumn 82, Issue 6, 2014, Pages 2337-2344

  Smyth, Danielle ^a,f   Cameron, Ainslie ^a   Davies, Mark R ^b,c   McNeilly, Celia ^a   Hafner, Louise ^d   Sriprakash, Kadaba S ^a   McMillan, David J ^a,e  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^e UNIVERSITY OF THE SUNSHINE COAST   (Australia)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; BACTERIAL PROTEIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DRSG PROTEIN; PROLINE; SECRETORY PROTEIN; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; BACTERICIDAL ACTIVITY; BIOLOGICAL ACTIVITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOCOCCUS DYSGALACTIAE; STREPTOCOCCUS DYSGALACTIAE SUBSP EQUISIMILIS; WESTERN BLOTTING; ANIMAL; BACTERIAL COUNT; CELL DEATH; DRUG EFFECTS; ERYTHROCYTE; METABOLISM; PHYSIOLOGY; SHEEP; STREPTOCOCCUS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL DEATH; COLONY COUNT, MICROBIAL; ERYTHROCYTES; RECOMBINANT PROTEINS; SHEEP; STREPTOCOCCUS;

EID: 84900422314     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01411-13     Document Type: Article

References (51)

1. Brogden KA. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3:238-250. http://dx.doi.org/10.1038/nrmicro1098.
2. Niyonsaba F, Iwabuchi K, Matsuda H, Ogawa H, Nagaoka I. 2002. Epithelial cell-derived human beta-defensin-2 acts as a chemotaxin for mast cells through a pertussis toxin-sensitive and phospholipase C-dependent pathway. Int. Immunol. 14:421-426. http://dx.doi.org/10.1093/intimm/14.4.421.
3. Lai Y, Gallo RL. 2009. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 30:131-141. http://dx.doi.org/10.1016/j.it.2008.12.003.
4. Peschel A, Sahl H. 2006. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4:529-536. http://dx.doi.org/10.1038/nrmicro1441.
5. Chhatwal GS, McMillan DJ, Talay SR. 2006. Pathogenicity factors in group C and G streptococci, p 213-221. In Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (ed), Gram-positive pathogens, 2nd ed. ASM Press, Washington, DC.
6. Efstratiou A. 1997. Pyogenic streptococci of Lancefield groups C and G as pathogens in man. Soc. Appl. Bacteriol. Symp. Ser. 26:72S-79S.
7. Hindsholm M, Schonheyder HC. 2002. Clinical presentation and outcome of bacteraemia caused by beta-haemolytic streptococci serogroup G. APMIS 110: 554-558. http://dx.doi.org/10.1034/j.1600-0463.2002.11007806.x.
8. Sylvetsky N, Raveh D, Schlesinger Y, Rudensky B, Yinnon AM. 2002. Bacteremia due to beta-hemolytic Streptococcus group G: increasing incidence and clinical characteristics of patients. Am. J. Med. 112:622-626. http://dx.doi.org/10.1016/S0002-9343(02)01117-8.
9. Ekelund K, Skinhoj P, Madsen J, Konradsen HB. 2005. Invasive group A, B, C and G streptococcal infections in Denmark 1999-2002: epidemiological and clinical aspects. Clin. Microbiol. Infect. 11:569-576. http://dx.doi.org/10.1111/j.1469-0691.2005.01169.x.
10. Fernie-King BA, Seilly DJ, Willers C, Wurzner R, Davies A, Lachmann PJ. 2001. Streptococcal inhibitor of complement (SIC) inhibits the membrane attack complex by preventing uptake of C567 onto cell membranes. Immunology 103:390-398. http://dx.doi.org/10.1046/j.1365-2567.2001.01249.x.
11. Akesson P, Sjoholm AG, Bjorck L. 1996. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J. Biol. Chem. 271:1081-1088. http://dx.doi.org/10.1074/jbc.271.2.1081.
12. Fernie-King BA, Seilly DJ, Lachmann PJ. 2004. The interaction of streptococcal inhibitor of complement (SIC) and its proteolytic fragments with the human beta defensins. Immunology 111:444-452. http://dx.doi.org/10.1111/j.0019-2805.2004.01837.x.
13. Frick IM, Nordin SL, Baumgarten M, Morgelin M, Sorensen OE, Olin AI, Egesten A. 2011. Constitutive and inflammation-dependent antimicrobial peptides produced by epithelium are differentially processed and inactivated by the commensal Finegoldia magna and the pathogen Streptococcus pyogenes. J. Immunol. 187:4300-4309. http://dx.doi.org/10.4049/jimmunol.1004179.
14. Egesten A, Eliasson M, Johansson HM, Olin AI, Morgelin M, Mueller A, Pease JE, Frick IM, Bjorck L. 2007. The CXC chemokine MIG/CXCL9 is important in innate immunity against Streptococcus pyogenes. J. Infect. Dis. 195:684-693. http://dx.doi.org/10.1086/510857.
15. Binks M, Sriprakash KS. 2004. Characterization of a complementbinding protein, DRS, from strains of Streptococcus pyogenes containing the emm12 and emm55 genes. Infect. Immun. 72:3981-3986. http://dx.doi.org/10.1128/IAI.72.7.3981-3986.2004.
16. Hartas J, Sriprakash KS. 1999. Streptococcus pyogenes strains containing emm12 and emm55 possess a novel gene coding for distantly related SIC protein. Microb. Pathog. 26:25-33. http://dx.doi.org/10.1006/mpat.1998.0244.
17. Fernie-King BA, Seilly DJ, Binks MJ, Sriprakash KS, Lachmann PJ. 2007. Streptococcal DRS (distantly related to SIC) and SIC inhibit antimicrobial peptides, components of mucosal innate immunity: a comparison of their activities. Microbes Infect. 9:300-307. http://dx.doi.org/10.1016/j.micinf.2006.12.006.
18. Shimomura Y, Okumura K, Murayama SY, Yagi J, Ubukata K, Kirikae T, Miyoshi-Akiyama T. 2011. Complete genome sequencing and analysis of a Lancefield group G Streptococcus dysgalactiae subsp. equisimilis strain causing streptococcal toxic shock syndrome (STSS). BMC Genomics 12:17. http://dx.doi.org/10.1186/1471-2164-12-17.
19. Davies MR, McMillan DJ, Beiko RG, Barroso V, Geffers R, Sriprakash KS, Chhatwal GS. 2007. Virulence profiling of Streptococcus dysgalactiae subspecies equisimilis isolated from infected humans reveals 2 distinct genetic lineages that do not segregate with their phenotypes or propensity to cause diseases. Clin. Infect. Dis. 44:1442-1454. http://dx.doi.org/10.1086/516780.
20. Minami M, Ichikawa M, Matsui H, Hata N, Wakiyama N, Matsumoto M, Ohta M, Hasegawa T. 2011. Prevalence of a streptococcal inhibitor of a complement-mediated cell lysis-like gene (sicG) in Streptococcus dysgalactiae subsp. equisimilis. Curr. Microbiol. 62:884-887. http://dx.doi.org/10.1007/s00284-010-9798-8.
21. Ahmad Y, Gertz RE, Jr, Li Z, Sakota V, Broyles LN, Van Beneden C, Facklam R, Shewmaker PL, Reingold A, Farley MM, Beall BW. 2009. Genetic relationships deduced from emm and multilocus sequence typing of invasive Streptococcus dysgalactiae subsp. equisimilis and S. canis recovered from isolates collected in the United States. J. Clin. Microbiol. 47: 2046-2054. http://dx.doi.org/10.1128/JCM.00246-09.
22. McMillan DJ, Kaul SY, Bramhachari PV, Smeesters PR, Vu T, Karmarkar MG, Shaila MS, Sriprakash KS. 2011. Recombination drives genetic diversification of Streptococcus dysgalactiae subspecies equisimilis in a region of streptococcal endemicity. PLoS One 6:e21346. http://dx.doi.org/10.1371/journal.pone.0021346.
23. McDonald M, Towers RJ, Andrews RM, Carapetis JR, Currie BJ. 2007. Epidemiology of Streptococcus dysgalactiae subsp. equisimilis in tropical communities, Northern Australia. Emerg. Infect. Dis. 13:1694-1700. http://dx.doi.org/10.3201/eid1311.061258.
24. Pinho MD, Melo-Cristino J, Ramirez M. 2006. Clonal relationships between invasive and noninvasive Lancefield group C and G streptococci and emm-specific differences in invasiveness. J. Clin. Microbiol. 44:841-846. http://dx.doi.org/10.1128/JCM.44.3.841-846.2006.
25. McMillan DJ, Bessen DE, Pinho M, Ford C, Hall GS, Melo-Cristino J, Ramirez M. 2010. Population genetics of Streptococcus dysgalactiae subspecies equisimilis reveals widely dispersed clones and extensive recombination. PLoS One 5:e11741. http://dx.doi.org/10.1371/journal.pone.0011741.
26. Sambrook J, Russell DW. 2006. The condensed protocols from molecular cloning: a laboratory manual, p 265-268. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R. 2010. A new bioinformatics analysis tools frame work at EMBL-EBI. Nucleic Acids Res. 38:W695-W699. http://dx.doi.org/10.1093/nar/gkq313.
28. Heger A, Holm L. 2000. Rapid automatic detection and alignment of repeats in protein sequences. Proteins 41:224-237. http://dx.doi.org/10.1002/1097-0134(20001101)41:2<224::AID-PROT70>l3.0.CO;2-Z.
29. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7:539. http://dx.doi.org/10.1038/msb.2011.75.
30. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
31. McMillan DJ, Davies MR, Good MF, Sriprakash KS. 2004. Immune response to superoxide dismutase in group A streptococcal infection. FEMS Immunol. Med. Microbiol. 40:249-256. http://dx.doi.org/10.1016/S0928-8244(04)00003-3.
32. Binks MJ, Fernie-King BA, Seilly DJ, Lachmann PJ, Sriprakash KS. 2005. Attribution of the various inhibitory actions of the streptococcal inhibitor of complement (SIC) to regions within the molecule. J. Biol. Chem. 280:20120-20125. http://dx.doi.org/10.1074/jbc.M414194200.
33. Murakami M, Ohtake T, Dorschner RA, Schittek B, Garbe C, Gallo RL. 2002. Cathelicidin anti-microbial peptide expression in sweat, an innate defense system for the skin. J. Invest. Dermatol. 119:1090-1095. http://dx.doi.org/10.1046/j.1523-1747.2002.19507.x.
34. Oppegaard O, Mylvaganam H, Skrede S, Langeland N, Kittang BR. 2014. Sequence diversity of sicG among group C and G Streptococcus dysgalactiae subspecies equisimilis isolates associated with human infections in western Norway. Eur. J. Clin. Microbiol. Infect. Dis. 33:273-277. http://dx.doi.org/10.1007/s10096-013-1955-0.
35. Davies MR, Tran TN, McMillan DJ, Gardiner DL, Currie BJ, Sriprakash KS. 2005. Inter-species genetic movement may blur the epidemiology of streptococcal diseases in endemic regions. Microbes Infect. 7:1128-1138. http://dx.doi.org/10.1016/j.micinf.2005.03.018.
36. Bessen DE, Hollingshead SK. 1995. Horizontal transfer and mosaic-like emm gene structures in group A streptococci. Dev. Biol. Stand. 85:169-173.
37. Davies MR, Shera J, Van Domselaar GH, Sriprakash KS, McMillan DJ. 2009. A novel integrative conjugative element mediates genetic transfer from group G streptococcus to other beta-hemolytic streptococci. J. Bacteriol. 191:2257-2265. http://dx.doi.org/10.1128/JB.01624-08.
38. Beres SB, Musser JM. 2007. Contribution of exogenous genetic elements to the group A Streptococcus metagenome. PLoS One 2:e800. http://dx.doi.org/10.1371/journal.pone.0000800.
39. Sitkiewicz I, Green NM, Guo N, Mereghetti L, Musser JM. 2011. Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins. BMC Microbiol. 11:65. http://dx.doi.org/10.1186/1471-2180-11-65.
40. Banks DJ, Beres SB, Musser JM. 2002. The fundamental contribution of phages to GAS evolution, genome diversification and strain emergence. Trends Microbiol. 10:515-521. http://dx.doi.org/10.1016/S0966-842X(02)02461-7.
41. Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, Henningham A, McArthur JD, Dinkla K, Aziz RK, Kansal RG, Simpson AJ, Buchanan JT, Chhatwal GS, Kotb M, Nizet V. 2007. DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat. Med. 13:981-985. http://dx.doi.org/10.1038/nm1612.
42. Goshorn SC, Schlievert PM. 1989. Bacteriophage association of streptococcal pyrogenic exotoxin type C. J. Bacteriol. 171:3068-3073.
43. Green NM, Zhang S, Porcella SF, Nagiec MJ, Barbian KD, Beres SB, LeFebvre RB, Musser JM. 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. http://dx.doi.org/10.1086/430618.
44. Franken C, Haase G, Brandt C, Weber-Heynemann J, Martin S, Lammler C, Podbielski A, Lutticken R, Spellerberg B. 2001. Horizontal gene transfer and host specificity of beta-haemolytic streptococci: the role of a putative composite transposon containing scpB and lmb. Mol. Microbiol. 41:925-935. http://dx.doi.org/10.1046/j.1365-2958.2001.02563.x.
45. Sriprakash KS, Hartas J. 1997. Genetic mosaic upstream of scpG in human group G streptococci contains sequences from group A streptococcal virulence regulon. Adv. Exp. Med. Biol. 418:749-751. http://dx.doi.org/10.1007/978-1-4899-1825-3_176.
46. Sagar V, Kumar R, Ganguly NK, Menon T, Chakraborti A. 2007. DRS is far less divergent than streptococcal inhibitor of complement of group A streptococcus. J. Bacteriol. 189:2933-2935. http://dx.doi.org/10.1128/JB.01619-06.
47. Hoe NP, Vuopio-Varkila J, Vaara M, Grigsby D, De Lorenzo D, Fu YX, Dou SJ, Pan X, Nakashima K, Musser JM. 2001. Distribution of streptococcal inhibitor of complement variants in pharyngitis and invasive isolates in an epidemic of serotype M1 group A Streptococcus infection. J. Infect. Dis. 183:633-639. http://dx.doi.org/10.1086/318543.
48. Kay BK, Williamson MP, Sudol M. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14:231-241. http://dx.doi.org/10.1096/fj.1530-6860.
49. Mayer BJ, Eck MJ. 1995. SH3 domains. Minding your p's and q's. Curr. Biol. 5:364-367.
50. Musacchio A, Saraste M, Wilmanns M. 1994. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat. Struct. Biol. 1:546-551. http://dx.doi.org/10.1038/nsb0894-546.
51. Williamson MP. 1994. The structure and function of proline-rich regions in proteins. Biochem. J. 15:249-260.