Group A streptococcus secreted esterase hydrolyzes platelet-activating factor to impede neutrophil recruitment and facilitate innate immune evasion

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Liu, Mengyao ^a   Zhu, Hui ^a,b   Li, Jinquan ^a,c   Garcia, Cristiana C ^d   Feng, Wenchao ^a   Kirpotina, Liliya N ^a   Hilmer, Jonathan ^a   Tavares, Luciana P ^d   Layton, Arthur W ^e   Quinn, Mark T ^a   Bothner, Brian ^a   Teixeira, Mauro M ^d   Lei, Benfang ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^e Montana Veterinary Diagnostic Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; BACTERIAL ENZYME; ESTERASE; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CELL ACTIVATION; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HISTOLOGY; HUMAN; HUMAN CELL; HYDROLYSIS; INNATE IMMUNITY; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; SKIN INFECTION; STREPTOCOCCUS GROUP A; ANIMAL; BACTERIAL SKIN DISEASE; CLINICAL TRIAL; ENZYMOLOGY; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; MULTICENTER STUDY; PATHOGENICITY; PATHOLOGY; SECRETION; SKIN; STREPTOCOCCUS;

BACTERIA (MICROORGANISMS); MUS; STREPTOCOCCUS SP. 'GROUP A';

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ANIMALS; FEMALE; GENE DELETION; HUMANS; IMMUNITY, INNATE; MALE; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; PLATELET ACTIVATING FACTOR; SKIN; SKIN DISEASES, BACTERIAL; STREPTOCOCCUS;

EID: 84861214601     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002624     Document Type: Article

References (58)

1. Carapetis JR, Steer AC, Mulholland EK, Weber M, (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5: 685-694.
2. Hidalgo-Grass C, Mishalian I, Dan-Goor M, Belotserkovsky I, Eran Y, et al. (2006) A streptococcal protease that degrades CXC chemokines and impairs bacterial clearance from infected tissues. EMBO J 25: 4628-4637.
3. Edwards RJ, Taylor GW, Ferguson M, Murray S, Rendell N, et al. (2005) Specific C-terminal cleavage and inactivation of interleukin-8 by invasive disease isolates of Streptococcus pyogenes. J Infect Dis 192: 783-790.
4. 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.
5. Zinkernagel AS, Timmer AM, Pence MA, Locke JB, Buchanan JT, et al. (2008) The IL-8 protease SpyCEP/ScpC of group A Streptococcus promotes resistance to neutrophil killing. Cell Host Microbe 4: 170-178.
6. Perez-Casal J, Caparon MG, Scott JR, (1992) Introduction of the emm6 gene into an emm-deleted strain of Streptococcus pyogenes restores its ability to resist phagocytosis. Res Microbiol 143: 549-558.
7. Ashbaugh CD, Moser TJ, Shearer MH, White GL, Kennedy RC, 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.
8. Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, et al. (2007) DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 13: 981-985.
9. Lei B, DeLeo FR, Hoe NP, Graham MR, Mackie SM, et al. (2001) Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis. Nat Med 7: 1298-1305.
10. von Pawel-Rammingen U, Johansson BP, Björck L, (2002) IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J 21: 1607-1615.
11. Timmer AM, Timmer JC, Pence MA, Hsu LC, Ghochani M, et al. (2009) Streptolysin O promotes group A Streptococcus immune evasion by accelerated macrophage apoptosis. J Biol Chem 284: 862-871.
12. Miyoshi-Akiyama T, Takamatsu D, Koyanagi M, Zhao J, Imanishi K, et al. (2005) Cytocidal effect of Streptococcus pyogenes on mouse neutrophils in vivo and the critical role of streptolysin S. J Infect Dis 192: 107-116.
13. Heath A, DiRita VJ, Barg NL, Engleberg NC, (1999) A two-component regulatory system, CsrR-CsrS, represses expression of three Streptococcus pyogenes virulence factors, hyaluronic acid capsule, streptolysin S, and pyrogenic exotoxin B. Infect Immun 67: 5298-5305.
14. Federle MJ, McIver KS, Scott JR, (1999) A Response Regulator That Represses Transcription of Several Virulence Operons in the Group A Streptococcus. J Bacteriol 181: 3649-3657.
15. Ikebe T, Ato M, Matsumura T, Hasegawa H, Sata T, et al. (2010) Highly frequent mutations in negative regulators of multiple virulence genes in group A streptococcal toxic shock syndrome isolates. PLoS Pathog 6: e1000832.
16. Engleberg NC, Heath A, Miller A, Rivera C, DiRita VJ, (2001) 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 183: 1043-1054.
17. Cole JN, McArthur JD, McKay FC, Sanderson-Smith ML, Cork AJ, et al. (2006) Trigger for group A streptococcal M1T1 invasive disease. FASEB J 20: 1745-1747.
18. Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM, (2006) Genome-Wide Analysis of Group A Streptococci Reveals a Mutation That Modulates Global Phenotype and Disease Specificity. PloS Pathog 2: 41-49.
19. Aziz RK, Pabst MJ, Jeng A, Kansal R, Low DE, et al. (2004) Invasive M1T1 group A Streptococcus undergoes a phase-shift in vivo to prevent proteolytic degradation of multiple virulence factors by SpeB. Mol Microbiol 51: 123-134.
20. Engleberg NC, Heath A, Vardaman K, DiRita VJ, (2004) Contribution of CsrR-regulated virulence factors to the progress and outcome of murine skin infections by Streptococcus pyogenes. Infect Immun 72: 623-628.
21. Bakleh M, Wold LE, Mandrekar JN, Harmsen WS, Dimashkieh HH, et al. (2005) Correlation of histopathologic findings with clinical outcome in necrotizing fasciitis. Clin Infect Dis 40: 410-414.
22. Cockerill FR 3rd, Thompson RL, Musser JM, Schlievert PM, Talbot J, et al. (1999) Molecular, serological, and clinical features of 16 consecutive cases of invasive streptococcal disease. Clin Infect Dis 26: 1448-1458.
23. Taylor FB Jr, Bryant AE, Blick KE, Hack E, Jansen PM, et al. (1999) Staging of the baboon response to group A streptococci administered intramuscularly: a descriptive study of the clinical symptoms and clinical chemical response patterns. Clin Infect Dis 29: 167-177.
24. Hanahan DJ, Demopoulos CA, Liehr J, Pinckard RN, (1980) Identification of platelet activating factor isolated from rabbit basophils as acetyl glyceryl ether phosphorylcholine. J Biol Chem 255: 5514-5516.
25. Chao W, Olson MS, (1993) Platelet-activating factor: receptors and signal transduction. Biochem J 292: 617-629.
26. Venable ME, Zimmerman GA, McIntyre TM, Prescott SM, (1993) Platelet-activating factor: a phospholipid autacoid with diverse actions. J Lipid Res 34: 691-702.
27. Benveniste J, Henson PM, Cochrane CG, (1972) Leukocyte-dependent histamine release from rabbit platelets. The role of IgE, basophils, and a platelet-activating factor. J Exp Med 136: 1356-1377.
28. Shaw JO, Pinckard RN, Ferrigni KS, McManus LM, Hanahan DJ, (1981) Activation of human neutrophils with 1-O-hexadecyl/octadecyl-2-acetyl-sn-glycerol-3-phosphorylcholine (platelet activating factor). J Immunol 127: 1250-1255.
29. Honda Z, Nakamura M, Miki I, Minami M, Watanabe T, et al. (1991) Cloning by functional expression of platelet-activating factor receptor from guinea-pig lung. Nature 349: 342-346.
30. Ishii S, Kuwaki T, Nagase T, Maki K, Tashiro F, et al. (1998) Impaired anaphylactic responses with intact sensitivity to endotoxin in mice lacking a platelet-activating factor receptor. J Exp Med 187: 1779-1788.
31. Tjoelker LW, Wilder C, Eberhardt C, Stafforini DM, Dietsch G, et al. (1995) Anti-inflammatory properties of a platelet-activating factor acetylhydrolase. Nature 374: 549-553.
32. Hattori K, Adachi H, Matsuzawa A, Yamamoto K, Tsujimoto M, et al. (1996) cDNA cloning and expression of intracellular platelet-activating factor (PAF) acetylhydrolase II: Its homology with plasma PAF acetylhydrolase. J Biol Chem 271: 33032-33038.
33. Hattori M, Arai H, Inoue K, (1993) Purification and characterization of bovine brain platelet-activating factor acetylhydrolase. J Biol Chem 268: 18748-18753.
34. Stafforini DM, Prescott SM, Zimmerman GA, McIntyre TM, (1996) Mammalian platelet-activating factor acetylhydrolases. Biochim Biophys Acta 1301: 161-173.
35. Stafforini DM, McIntyre TM, Zimmerman GA, Prescott SM, (1997) Platelet-activating factor acetylhydrolases. J Biol Chem 272: 17895-17898.
36. Foulks JM, Weyrich AS, Zimmerman GA, McIntyre TM, (2008) A yeast PAF acetylhydrolase ortholog suppresses oxidative death. Free Radic Biol Med 45: 434-442.
37. Yang J, Zhang Y, Xu J, Geng Y, Chen X, et al. (2009) Serum activity of platelet-activating factor acetylhydrolase is a potential clinical marker for leptospirosis pulmonary hemorrhage. PLoS One 4: e4181.
38. Navarro-Fernández J, Nechitaylo TY, Guerrero JA, Golyshina OV, García-Carmona F, et al. (2011) A novel platelet-activating factor acetylhydrolase discovered in a metagenome from the earthworm-associated microbial community. Environ Microbiol 13: 3036-3046.
39. Liu M, Zhu H, Zhang J, Lei B, (2007) Active and passive immunizations with the streptococcal esterase Sse protect mice against subcutaneous infection with group A streptococci. Infect Immun 75: 3651-3657.
40. Zhu H, Liu M, Sumby P, Lei B, (2009) The secreted esterase of group a streptococcus is important for invasive skin infection and dissemination in mice. Infect Immun 77: 5225-5232.
41. Xie G, Liu M, Zhu H, Lei B, (2008) Esterase SeE of Streptococcus equi ssp. equi is a novel nonspecific carboxylic ester hydrolase. FEMS Microbiol Lett 289: 181-186.
42. Yost CC, Weyrich AS, Zimmerman GA, (2010) The platelet activating factor (PAF) signaling cascade in systemic inflammatory responses. Biochimie 92: 692-697.
43. Aarsman AJ, Neys FW, Van den Bosch H, (1991) Catabolism of platelet-activating factor and its acyl analog. Differentiation of the activities of lysophospholipase and platelet-activating-factor acetylhydrolase. Eur J Biochem 200: 187-193.
44. Bradley PP, Priebat DA, Christensen RD, Rothstein G, (1982) Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78: 206-209.
45. Treviño J, Perez N, Ramirez-Peña E, Liu Z, Shelburne SA, et al. (2009) CovS simultaneously activates and inhibits the CovR-mediated repression of distinct subsets of group A Streptococcus virulence factor-encoding genes. Infect Immun 77: 3141-3149.
46. Kurupati P, Turner CE, Tziona I, Lawrenson RA, Alam FM, et al. (2010) Chemokine-cleaving Streptococcus pyogenes protease SpyCEP is necessary and sufficient for bacterial dissemination within soft tissues and the respiratory tract. Mol Microbiol 76: 1387-1397.
47. Turner CE, Kurupati P, Wiles S, Edwards RJ, Sriskandan S, (2009) Impact of immunization against SpyCEP during invasive disease with two streptococcal species: Streptococcus pyogenes and Streptococcus equi. Vaccine 27: 4923-4929.
48. Sumby P, Zhang S, Whitney AR, Falugi F, Grandi G, et al. (2008) A chemokine-degrading extracellular protease made by group A Streptococcus alters pathogenesis by enhancing evasion of the innate immune response. Infect Immun 76: 978-985.
49. Ji Y, Carlson B, Kondagunta A, Cleary PP, (1997) Intranasal immunization with C5a peptidase prevents nasopharyngeal colonization of mice by the group A Streptococcus. Infect Immun 65: 2080-2087.
50. van Zoelen MA, Florquin S, Meijers JC, de Beer R, de Vos AF, et al. (2008) Platelet-activating factor receptor contributes to host defense against Pseudomonas aeruginosa pneumonia but is not essential for the accompanying inflammatory and procoagulant response. J Immunol 180: 3357-3365.
51. Branger J, Wieland CW, Florquin S, Maris NA, Pater JM, et al. (2004) Platelet-activating factor receptor-deficient mice show an unaltered clearance of nontypeable Haemophilus influenzae from their respiratory tract. Shock 22: 543-547.
52. Rijneveld AW, Weijer S, Florquin S, Speelman P, Shimizu T, et al. (2004) Improved host defense against pneumococcal pneumonia in platelet-activating factor receptor-deficient mice. J Infect Dis 189: 711-716.
53. Moreno SE, Alves-Filho JC, Rios-Santos F, Silva JS, Ferreira SH, et al. (2006) Signaling via platelet-activating factor receptors accounts for the impairment of neutrophil migration in polymicrobial sepsis. J Immunol 177: 1264-1271.
54. Hermoso JA, Lagartera L, González A, Stelter M, García P, et al. (2005) Insights into pneumococcal pathogenesis from the crystal structure of the modular teichoic acid phosphorylcholine esterase Pce. Nat Struct Mol Biol 12: 533-538.
55. Lee YM, Hybertson BM, Cho HG, Repine JE, (2002) Platelet-activating factor induces lung inflammation and leak in rats: hydrogen peroxide production along neutrophil-lung endothelial cell interfaces. J Lab Clin Med 140: 312-319.
56. Bussolati B, Mariano F, Cignetti A, Guarini A, Cambi V, et al. (1998) Platelet-activating factor synthesized by IL-12-stimulated polymorphonuclear neutrophils and NK cells mediates chemotaxis. J Immunol 161: 1493-1500.
57. Siemsen DW, Schepetkin IA, Kirpotina LN, Lei B, Quinn MT, (2007) Neutrophil isolation from nonhuman species. Methods Mol Biol 412: 21-34.
58. Kirpotina LN, Khlebnikov AI, Schepetkin IA, Ye RD, Rabiet MJ, et al. (2010) Identification of novel small-molecule agonists for human formyl peptide receptors and pharmacophore models of their recognition. Mol Pharmacol 77: 159-170.