Analysis of the Staphylococcus aureus abscess proteome identifies antimicrobial host proteins and bacterial stress responses at the host-pathogen interface

Pathogens and Disease

Volumn 69, Issue 1, 2013, Pages 36-48

  Attia, Ahmed S ^a,c   Cassat, James E ^a   Aranmolate, Sheg O ^a   Zimmerman, Lisa J ^a   Boyd, Kelli L ^a,b   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c CAIRO UNIVERSITY   (Egypt)

Author keywords

Innate immunity; Pathogenesis; Proteomics; Staphylococcus aureus

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; ALPHA 1 ANTITRYPSIN; BETA2 GLYCOPROTEIN 1; CD18 ANTIGEN; FILAMIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HEAT SHOCK PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; HISTONE H4; INTER ALPHA TRYPSIN INHIBITOR; IRON SULFUR PROTEIN; LACTOFERRIN; LAMIN B; LIPOCORTIN 1; MYELOBLASTIN; MYELOPEROXIDASE; MYOSIN HEAVY CHAIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PEPTIDYLPROLYL ISOMERASE; PEROXIREDOXIN 5; PHOSPHOGLUCONATE DEHYDROGENASE; PLASMINOGEN; PROTEIN 14 3 3; PROTEIN S 100; PROTEOME; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 2; SELENIUM BINDING PROTEIN; SERUM AMYLOID A; TALIN; UNCLASSIFIED DRUG; UNIVERSAL STRESS PROTEIN 2; IMMUNOLOGIC FACTOR; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELLULAR STRESS RESPONSE; COLONY FORMING UNIT; CONTROLLED STUDY; DNA FLANKING REGION; FEMALE; HISTOLOGY; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATORY INFILTRATE; INNATE IMMUNITY; KIDNEY ABSCESS; KIDNEY INJURY; LIQUID CHROMATOGRAPHY; MOUSE; NEUTROPENIA; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEOMICS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; SURVIVAL RATE; TANDEM MASS SPECTROMETRY; ABSCESS; ANIMAL; CHEMISTRY; DISEASE MODEL; IMMUNOLOGY; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; SKIN;

ABSCESS; ANIMALS; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; IMMUNOLOGIC FACTORS; MICE; PROTEOME; SKIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84900320307     PISSN: None     EISSN: 2049632X     Source Type: Journal    
DOI: 10.1111/2049-632X.12063     Document Type: Article

References (51)

1. Anderson KL, Roberts C, Disz T, Vonstein V, Hwang K, Overbeek R, Olson PD, Projan SJ & Dunman PM (2006) Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol 188: 6739-6756.
2. Attia AS, Benson MA, Stauff DL, Torres VJ & Skaar EP (2010) Membrane damage elicits an immunomodulatory program in Staphylococcus aureus. PLoS Pathog 6: e1000802.
3. Bae T & Schneewind O (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
4. Bonner RF, Emmert-Buck M, Cole K, Pohida T, Chuaqui R, Goldstein S & Liotta LA (1997) Laser capture microdissection: molecular analysis of tissue. Science 278: 1481, 1483.
5. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y & Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
6. Bubeck Wardenburg J, Williams WA & Missiakas D (2006) Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. P Natl Acad Sci USA 103: 13831-13836.
7. Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23: 3393-3404.
8. Cheng AG, DeDent AC, Schneewind O & Missiakas D (2011) A play in four acts: Staphylococcus aureus abscess formation. Trends Microbiol 19: 225-232.
9. Chien Y, Manna AC, Projan SJ & Cheung AL (1999) SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J Biol Chem 274: 37169-37176.
10. Corbin BD, Seeley EH, Raab A et al. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962-965.
11. Crosse AM, Greenway DL & England RR (2000) Accumulation of ppGpp and ppGp in Staphylococcus aureus 8325-4 following nutrient starvation. Lett Appl Microbiol 31: 332-337.
12. Czuprynski CJ, Brown JF, Maroushek N, Wagner RD & Steinberg H (1994) Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J Immunol 152: 1836-1846.
13. Drumm JE, Mi K, Bilder P et al. (2009) Mycobacterium tuberculosis universal stress protein Rv2623 regulates bacillary growth by ATP-Binding: requirement for establishing chronic persistent infection. PLoS Pathog 5: e1000460.
14. Duthie ES & Lorenz LL (1952) Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6: 95-107.
15. Ermert D, Urban CF, Laube B, Goosmann C, Zychlinsky A, Brinkmann V (2009) Mouse neutrophil extracellular traps in microbial infections. J Innate Immun 1: 181-193.
16. Francois P, Scherl A, Hochstrasser D & Schrenzel J (2010) Proteomic approaches to study Staphylococcus aureus pathogenesis. J Proteomics 73: 701-708.
17. Gustavsson N, Diez A & Nystrom T (2002) The universal stress protein paralogues of Escherichia coli are co-ordinately regulated and co-operate in the defence against DNA damage. Mol Microbiol 43: 107-117.
18. Ham AJ, Caprioli RM & Gross ML (2005) Proteolytic digestion protocols. The Encyclopedia of Mass Spectrometry, Vol. 2 (Caprioloi RM, Gross ML, eds), pp. 10-17. Elsevier Ltd, Oxford, UK.
19. Hestdal K, Ruscetti FW, Ihle JN, Jacobsen SE, Dubois CM, Kopp WC, Longo DL & Keller JR (1991) Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J Immunol 147: 22-28.
20. Howell SJ, Wilk D, Yadav SP & Bevins CL (2003) Antimicrobial polypeptides of the human colonic epithelium. Peptides 24: 1763-1770.
21. Hussain M, Becker K, von Eiff C, Schrenzel J, Peters G & Herrmann M (2001) Identification and characterization of a novel 38.5-kilodalton cell surface protein of Staphylococcus aureus with extended-spectrum binding activity for extracellular matrix and plasma proteins. J Bacteriol 183: 6778-6786.
22. Jacobsen F, Baraniskin A, Mertens J, Mittler D, Mohammadi-Tabrisi A et al. (2005) Activity of histone H1.2 in infected burn wounds. J Antimicrob Chemother 55: 735-741.
23. Klevens RM, Morrison MA, Nadle J et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771.
24. 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.
25. Kvint K, Nachin L, Diez A & Nystrom T (2003) The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6: 140-145.
26. Kylvaja R, Kankainen M, Holm L & Westerlund-Wikstrom B (2011) Adhesive polypeptides of Staphylococcus aureus identified using a novel secretion library technique in Escherichia coli. BMC Microbiol 11: 117.
27. Lee LY, Miyamoto YJ, McIntyre BW, Hook M, McCrea KW, McDevitt D & Brown EL (2002) The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J Clin Invest 110: 1461-1471.
28. Lee DY, Huang CM, Nakatsuji T, Thiboutot D, Kang SA, Monestier M & Gallo RL (2009) Histone H4 is a major component of the antimicrobial action of human sebocytes. J Invest Dermatol 129: 2489-2496.
29. Liao L, Cheng D, Wang J, Duong DM, Losik TG, Gearing M, Rees HD, Lah JJ, Levey AI & Peng J (2004) Proteomic characterization of postmortem amyloid plaques isolated by laser capture microdissection. J Biol Chem 279: 37061-37068.
30. Liu WT, Karavolos MH, Bulmer DM, Allaoui A, Hormaeche RD, Lee JJ & Khan CM (2007) Role of the universal stress protein UspA of Salmonella in growth arrest, stress and virulence. Microb Pathog 42: 2-10.
31. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
32. 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.
33. Malone CL, Boles BR, Lauderdale KJ, Thoendel M, Kavanaugh JS & Horswill AR (2009) Fluorescent reporters for Staphylococcus aureus. J Microbiol Methods 77: 251-260.
34. Marchler-Bauer A, Lu S, Anderson JB et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
35. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, Joachmiak A, Missiakas DM & Schneewind O (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
36. Nachin L, Nannmark U & Nystrom T (2005) Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol 187: 6265-6272.
37. Nystrom T & Neidhardt FC (1994) Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol Microbiol 11: 537-544.
38. O'Toole R & Williams HD (2003) Universal stress proteins and Mycobacterium tuberculosis. Res Microbiol 154: 387-392.
39. Parseghian MH & Luhrs KA (2006) Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 84: 589-604.
40. Rekhter MD & Chen J (2001) Molecular analysis of complex tissues is facilitated by laser capture microdissection: critical role of upstream tissue processing. Cell Biochem Biophys 35: 103-113.
41. Resch A, Leicht S, Saric M, Pasztor L, Jakob A, Gotz F & Nordheim A (2006) Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6: 1867-1877.
42. Singh VK, Jayaswal RK & Wilkinson BJ (2001) Cell wall-active antibiotic induced proteins of Staphylococcus aureus identified using a proteomic approach. FEMS Microbiol Lett 199: 79-84.
43. Tabb DL, Fernando CG & Chambers MC (2007) MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J Proteome Res 6: 654-661.
44. Tenover FC & Goering RV (2009) Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J Antimicrob Chemother 64: 441-446.
45. Torres VJ, Stauff DL, Pishchany G, Bezbradica JS, Gordy LE, Iturregui J, Anderson KL, Dunman PM, Joyce S & Skaar EP (2007) A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1: 109-119.
46. Tzianabos AO, Wang JY & Lee JC (2001) Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides. P Natl Acad Sci USA 98: 9365-9370.
47. Ventura CL, Higdon R, Hohmann L, Martin D, Kolker E, Liggitt HD, Skerrett SJ & Rubens CE (2008) Staphylococcus aureus elicits marked alterations in the airway proteome during early pneumonia. Infect Immun 76: 5862-5872.
48. Washburn MP, Wolters D & Yates JR 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247.
49. Wolf C, Hochgrafe F, Kusch H, Albrecht D, Hecker M & Engelmann S (2008) Proteomic analysis of antioxidant strategies of Staphylococcus aureus: diverse responses to different oxidants. Proteomics 8: 3139-3153.
50. Wolffe AP & Guschin D (2000) Review: chromatin structural features and targets that regulate transcription. J Struct Biol 129: 102-122.
51. Zhang B, Chambers MC & Tabb DL (2007) Proteomic parsimony through bipartite graph analysis improves accuracy and transparency. J Proteome Res 6: 3549-3557.