CpsY influences Streptococcus iniae cell wall adaptations important for neutrophil intracellular survival

Infection and Immunity

Volumn 80, Issue 5, 2012, Pages 1707-1715

  Allen, Jonathan P ^a,b   Neely, Melody N ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; BACTERIAL PROTEIN; METHIONINE; PEPTIDOGLYCAN; PROTEIN CPSY; UNCLASSIFIED DRUG;

ACETYLATION; ADAPTATION; ARTICLE; BACTERIAL CELL WALL; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; METABOLISM; NEUTROPHIL; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STREPTOCOCCUS INFECTION; STREPTOCOCCUS INIAE; TRANSCRIPTION REGULATION;

ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CELL WALL; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; NEUTROPHILS; PHAGOSOMES; PROMOTER REGIONS, GENETIC; STREPTOCOCCUS; TRANSCRIPTION FACTORS;

EID: 84861153316     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00027-12     Document Type: Article

References (86)

1. Agnew W, Barnes AC. 2007. Streptococcus iniae: an aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination. Vet. Microbiol. 122:1-15.
2. Allen JP, Neely MN. 2011. The Streptococcus iniae transcriptional regulator CpsY is required for protection from neutrophil-mediated killing and proper growth in vitro. Infect. Immun. 79:4638-4648.
3. Bera A, Biswas R, Herbert S, Gotz F. 2006. The presence of peptidoglycan O-acetyltransferase in various staphylococcal species correlates with lysozyme resistance and pathogenicity. Infect. Immun. 74:4598-4604.
4. Bera A, Herbert S, Jakob A, Vollmer W, Gotz F. 2005. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan Oacetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55:778-787.
5. Bernard E, et al. 2011. Characterization of O-acetylation of Nacetylglucosamine: a novel structural variation of bacterial peptidoglycan. J. Biol. Chem. 286:23950-23958.
6. Blackburn NT, Clarke AJ. 2002. Characterization of soluble and membrane-bound family 3 lytic transglycosylases from Pseudomonas aeruginosa. Biochemistry 41:1001-1013.
7. Boneca IG, et al. 2007. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U. S. A. 104:997-1002.
8. Borregaard N. 2010. Neutrophils, from marrow to microbes. Immunity 33:657-670.
9. Borregaard N, Cowland JB. 1997. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89:3503-3521.
10. Bryan JD, Liles R, Cvek U, Trutschl M, Shelver D. 2008. Global transcriptional profiling reveals Streptococcus agalactiae genes controlled by the MtaR transcription factor. BMC Genomics 9:607-619.
11. Buchanan JT, et al. 2008. Strain-associated virulence factors of Streptococcus iniae in hybrid-striped bass. Vet. Microbiol. 131:145-153.
12. Buchanan JT, et al. 2005. Streptococcus iniae phosphoglucomutase is a virulence factor and a target for vaccine development. Infect. Immun. 73:6935-6944.
13. Campanelli D, et al. 1990. Cloning of cDNA for proteinase 3: a serine protease, antibiotic, and autoantigen from human neutrophils. J. Exp. Med. 172:1709-1715.
14. Carroll SA, et al. 2003. Identification and characterization of a peptidoglycan hydrolase, MurA, of Listeria monocytogenes, a muramidase needed for cell separation. J. Bacteriol. 23:6801-6808.
15. Chan KG, et al. 2007. Role of D-alanylation of Streptococcus gordonii lipoteichoic acid in innate and adaptive immunity. Infect. Immun. 75: 3033-3042.
16. Cole A, et al. 2002. Cationic polypeptides are required for antibacterial activity of human airway fluid. J. Immunol. 169:6985-6991.
17. Cramer E, Breton-Gorius J. 1987. Ultrastructural localization of lysozyme in human neutrophils by immunogold. J. Leukoc. Biol. 41:242-247.
18. Crater DL, van de Rijn I. 1995. Hyaluronic acid synthesis operon (has) expression in group A streptococci. J. Biol. Chem. 270:18452-18458.
19. Crisostomo MI, et al. 2006. Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae. Mol. Microbiol. 61:1497-1509.
20. Eldar A, Bejerano Y, Livoff A, Horovitz A, Bercovier H. 1995. Experimental streptococcal meningo-encephalitis in cultured fish. Vet. Microbiol. 43.
21. Eldar A, et al. 1995. Streptococcus shiloi, the name for an agent causing septicemic infection in fish, is a junior synonym of Streptococcus iniae. Int. J. Syst. Bacteriol. 45:840-842.
22. Eldholm V, et al. 2010. The pneumococcal cell envelope stress-sensing system LiaFSR is activated by murein hydrolases and lipid II-interacting antibiotics. J. Bacteriol. 192:1761-1773.
23. Ernst CM, et al. 2009. The bacterial defensin resistance protein MprF consists of separable domains for lipid lysinylation and antimicrobial peptide repulsion. PLoS Pathog. 5:e1000660.
24. Fittipaldi N, et al. 2008. D-Alanylation of lipoteichoic acid contributes to the virulence of Streptococcus suis. Infect. Immun. 76:3587-3594.
25. Fuller JD, Bast DJ, Nizet V, Low DE, DE Azavedo JC. 2001. Streptococcus iniae virulence is associated with a distinct genetic profile. Infect. Immun. 69:1994-2000.
26. Ganz T. 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3:710-720.
27. Garcia DL, Dillard JP. 2006. AmiC functions as an N-acetylmuramyl-Lalanine amidase necessary for cell separation and can promote autolysis in Neisseria gonorrhoeae. J. Bacteriol. 188:7211-7221.
28. Haas W, Kaushal D, Sublett J, Obert C, Tuomanen EI. 2005. Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae. J. Bacteriol. 187:8205-8210.
29. Hanski E, Horwitz PA, Caparon MG. 1992. Expression of protein F, the fibronectin-binding protein of Streptococcus pyogenes JRS4, in heterologous streptococcal and enterococcal strains promotes their adherence to respiratory epithelial cells. Infect. Immun. 60:5119-5125.
30. Hayashi K. 1975. A rapid determination of sodium dodecyl sulfate with methylene blue. Anal. Biochem. 67:503-506.
31. Hebert L, et al. 2007. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect. Immun. 75:5390-5398.
32. Heidrich C, et al. 2001. Involvement of N-acetyl-muramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167-178.
33. Heidrich C, Ursinus A, Berger J, Schwarz H, Holtje JV. 2002. Effects of multiple deltions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J. Bacteriol. 184: 6093-6099.
34. Herbert S, et al. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3:e102.
35. Jabado N, et al. 2000. Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J. Exp. Med. 192:1237-1248.
36. Jordan S, et al. 2007. LiaRS-dependent gene expression is embedded in transition state regulation in Bacillus subtilis. Microbiology 153:2530-2540.
37. Kjeldsen L, Bainton DF, Sengelov H, Borregaard N. 1994. Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. Blood 83:799-807.
38. Klebanoff, S. J. 1999. Myeloperoxidase. Proc. Assoc. Am. Physicians 111: 383-389.
39. Kovacs M, et al. 2006. A functional dlt operon, encoding proteins required for incorporation of D-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J. Bacteriol. 188:5797-5805.
40. Kovaleva GY, Gelfand MS. 2007. Transcriptional regulation of the methionine and cysteine transport and metabolism in streptococci. FEMS Microbiol. Lett. 276:207-215.
41. Kramer NE, et al. 2008. Increased D-alanylation of lipoteichoic acid and a thickened septum are main determinants in the nisin resistance mechanism of Lactococcus lactis. Microbiology 154:1755-1762.
42. Kraus D, et al. 2008. The GraRS regulatory system controls Staphylococcus aureus susceptibility to antimicrobial host defenses. BMC Microbiol. 8:85.
43. Kristian SA, et al. 2005. D-Alanylation of teichoic acids promotes group a streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J. Bacteriol. 187:6719-6725.
44. Kristian SA, Durr M, Van Strijp JA, Neumeister B, Peschel A. 2003. MprF-mediated lysinylation of phospholipids in Staphylococcus aureus leads to protection against oxygen-independent neutrophil killing. Infect. Immun. 71:546-549.
45. Kuroda M, et al. 2003. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol. Microbiol. 49:807-821.
46. Laaberki MH, Pfeffer J, Clarke AJ, Dworkin J. 2011. O-acetylation of peptidoglycan is required for proper cell separation and S-layer anchoring in Bacillus anthracis. J. Biol. Chem. 286:5278-5288.
47. Lee WL, Harrison RE, Grinstein S. 2003. Phagocytosis by neutrophils. Microbes Infect. 5:1299-1306.
48. Li J, et al. 2010. The two-component regulatory system CiaRH contributes to the virulence of Streptococcus suis 2. Vet. Microbiol. 148: 99-104.
49. Li SY, Holtje JV, Young KD. 2004. Comparison of high-performance liquid chromatography and fluorophore-assisted carbohydrate electrophoresis methods for analyzing peptidoglycan composition of Escherichia coli. Anal. Biochem. 326:1-12.
50. Llull D, Lopez R, Garcia E. 2001. Genetic bases and medical relevance of capsular polysaccharide biosynthesis in pathogenic streptococci. Curr. Mol. Med. 1:475-491.
51. Lowe BA, Miller JD, Neely MN. 2007. Analysis of the polysaccharide capsule of the systemic pathogen Streptococcus iniae and its implications in virulence. Infect. Immun. 75:1255-1264.
52. Lyon WR, Gibson CM, Caparon MG. 1998. 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. 17:6263-6275.
53. Malech HL, Nauseef WM. 1997. Primary inherited defects in neutrophil function: etiology and treatment. Semin. Hematol. 34:279-290.
54. Meyrand M, et al. 2007. Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 153:3275-3285.
55. Miller JD, Neely MN. 2005. Large-scale screen highlights the importance of capsule for the systemic zoonotic pathogen Streptococcus iniae. Infect. Immun. 73:921-934.
56. Moynihan PJ, Clarke AJ. 2010. O-acetylation of peptidoglycan in gramnegative bacteria: identification and characterization of peptidoglycan Oacetyltransferase in Neisseria gonorrhoeae. J. Biol. Chem. 285:13264-13273.
57. Nash JA, Ballard TN, Weaver TE, Akinbi HT. 2006. The peptidoglycandegrading property of lysozyme is not required for bactericidal activity in vivo. J. Immunol. 177:519-526.
58. Oram JD, Reiter B. 1968. Inhibition of bacteria by lactoferrin and other iron-chelating agents. Biochim. Biophys. Acta 170:351-365.
59. Papayannopoulos V, Zychlinsky A. 2009. NETs: a new strategy for using old weapons. Trends Immunol. 30:513-521.
60. Payie KG, Strating H, Clarke AJ. 1996. The role of O-acetylation in the metabolism of peptidoglycan in Providencia stuartii. Microb. Drug Resist. 2:135-140.
61. Peschel A, et al. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J. Exp. Med. 193:1067-1076.
62. Pfeffer JM, Strating H, Weadge JT, Clarke AJ. 2006. Peptidoglycan O acetylation and autolysin profile of Enterococcus faecalis in the viable but nonculturable state. J. Bacteriol. 188:902-908.
63. Pietiainen M, et al. 2009. Transcriptome analysis of the responses of Staphylococcus aureus to antimicrobial peptides and characterization of the roles of vraDE and vraSR in antimicrobial resistance. BMC Genomics 10:429.
64. Poyart C, et al. 2003. Attenuated virulence of Streptococcus agalactiae deficient in D-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. Mol. Microbiol. 49:1615-1625.
65. Priyadarshini R, Popham DL, Young KD. 2006. Daughter cell separation by penicillin-binding proteins and peptidoglycan amidases in Escherichia coli. J. Bacteriol. 188:5345-5355.
66. Quach D, et al. 2009. The CiaR response regulator in group B Streptococcus promotes intracellular survival and resistance to innate immune defenses. J. Bacteriol. 191:2023-2032.
67. Ramanathan B, Davis EG, Ross CR, Blecha F. 2002. Cathelicidins: microbicidal activity, mechanisms of action, and roles in innate immunity. Microbes Infect. 4:361-372.
68. Rice KC, Bayles KW. 2008. Molecular control of bacterial death and lysis. Microbiol. Mol. Biol. Rev. 72:85-109.
69. Salvesen G, et al. 1987. Molecular cloning of human cathepsin G: structural similarity to mast cell and cytotoxic T lymphocyte proteinases. Biochemistry 26:2289-2293.
70. Samant S, Hsu FF, Lee H. 2009. The Bacillus anthracis MprF is required for synthesis of lysylphosphatidylglycerols and for resistance to cationic antimicrobial peptides. J. Bacteriol. 191:1311-1319.
71. Segal AW. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23:197-223.
72. Sinha S, et al. 1987. Primary structure of human neutrophil elastase. Proc. Natl. Acad. Sci. U. S. A. 84:2228-2232.
73. Sperandio B, et al. 2007. Control of methionine synthesis and uptake by MetR and homocysteine in Streptococcus mutans. J. Bacteriol. 189:7032-7044.
74. Staali L, Bauer S, Morgelin M, Bjorck L, Tapper H. 2006. Streptococcus pyogenes bacteria modulate membrane traffic in human neutrophils and selectively inhibit azurophilic granule fusion with phagosomes. Cell. Microbiol. 8:690-703.
75. Suntharalingam P, Senadheera MD, Mair RW, Levesque CM, Cvitkovitch DG. 2009. The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans. J. Bacteriol. 191:2973-2984.
76. Terao Y, et al. 2008. Group A streptococcal cysteine protease degrades C3 (C3b) and contributes to evasion of innate immunity. J. Biol. Chem. 283: 6253-6260.
77. Thedieck K, et al. 2006. The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol. Microbiol. 62:1325-1339.
78. Uehara T, Parzych KR, Dinh T, Bernhardt TG. 2010. Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolases. EMBO J. 29:1412-1422.
79. Urban CF, Lourido S, Zychlinsky A. 2006. How do microbes evade neutrophil killing? Cell. Microbiol. 8:1687-1696.
80. Veiga P, et al. 2007. SpxB regulates O-acetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J. Biol. Chem. 282:19342-19354.
81. Vollmer W, Tomasz A. 2002. Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect. Immun. 70:7176-7178.
82. Vollmer W, Tomasz A. 2000. The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J. Biol. Chem. 275:20496-20501.
83. Wang G, et al. 2010. Peptidoglycan deacetylation in Helicobacter pylori contributes to bacterial survival by mitigating host immune responses. Infect. Immun. 78:4660-4666.
84. Wecke T, Veith B, Ehrenreich A, Mascher T. 2006. Cell envelope stress response in Bacillus licheniformis: integrating comparative genomics, transcriptional profiling, and regulon mining to decipher a complex regulatory network. J. Bacteriol. 188:7500-7511.
85. Yajima A, et al. 2009. Contibution of phosphoglucosamine mutase to the resistance of Streptococcus gordonii DL1 to polymorphonuclear leukocyte killing. FEMS Microbiol. Lett. 297:196-202.
86. Young KD. 1996. A simple gel electrophoretic method for analyzing the muropeptide composition of bacterial peptidoglycan. J. Bacteriol. 178:3962-3966.