Staphylococcal adaptation to diverse physiologic niches: An overview of transcriptomic and phenotypic changes in different biological environments

Future Microbiology

Volumn 10, Issue 12, 2015, Pages 1981-1995

  Dastgheyb, Sana S ^a   Otto, Michael ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

gene expression; host pathogen interaction; niche adaptation; staphylococci

Indexed keywords

PROTEOME; TRANSCRIPTOME; VIRULENCE FACTOR; OXYGEN;

ADAPTATION; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BLOODSTREAM INFECTION; BONE; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; GENITAL SYSTEM; HOST PARASITE INTERACTION; INFECTIOUS ARTHRITIS; MORPHOLOGY; NONHUMAN; NOSE; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RESPIRATORY SYSTEM; REVIEW; STAPHYLOCOCCUS AUREUS; TRANSCRIPTOMICS; URINARY TRACT INFECTION; ENVIRONMENT; FOOD; GENE EXPRESSION PROFILING; HUMAN; PH; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ENVIRONMENT; FOOD; GENE EXPRESSION PROFILING; HUMANS; HYDROGEN-ION CONCENTRATION; OXYGEN; PHENOTYPE; PROTEOME; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL;

EID: 84948403018     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.15.116     Document Type: Review

References (152)

1. Gordon RJ, Lowy FD. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46(Suppl. 5), S350-S359 (2008).
2. Bore E, Langsrud S, Langsrud O, Rode TM, Holck A. Acid-shock responses in Staphylococcus aureus investigated by global gene expression analysis. Microbiology 153(Pt 7), 2289-2303 (2007).
3. Krismer B, Liebeke M, Janek D et al. Nutrient limitation governs Staphylococcus aureus metabolism and niche adaptation in the human nose. PLoS Pathog. 10(1), e1003862 (2014).
4. Resch A, Rosenstein R, Nerz C, Gotz F. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 71(5), 2663-2676 (2005).
5. King MD. Emergence of communityacquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann. Intern. Med. 144(5), 309 (2006).
6. Conway T, Schoolnik GK. Microarray expression profiling: capturing a genome-wide portrait of the transcriptome. Mol. Microbiol. 47(4), 879-889 (2003).
7. Rooijakkers SH, Van Kessel KP, Van Strijp JA. Staphylococcal innate immune evasion. Trends Microbiol. 13(12), 596-601 (2005).
8. Otto M. Staphylococcus aureus toxins. Curr. Opin. Microbiol. 17, 32-37 (2014).
9. Peschel A, Otto M. Phenol-soluble modulins and staphylococcal infection. Nat. Rev. Microbiol. 11(10), 667-673 (2013).
10. Queck SY, Jameson-Lee M, Villaruz AE et al. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell. 32(1), 150-158 (2008).
11. Recsei P, Kreiswirth B, O'reilly M, Schlievert P, Gruss A, Novick RP. Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Mol. Gen. Genet. 202(1), 58-61 (1986).
12. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol. Life Sci. 67(18), 3057-3071 (2010).
13. Li M, Diep BA, Villaruz AE et al. Evolution of virulence in epidemic communityassociated methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 106(14), 5883-5888 (2009).
14. Wang R, Braughton KR, Kretschmer D et al. Identification of novel cytolytic peptides as key virulence determinants for communityassociated MRSA. Nat. Med. 13(12), 1510-1514 (2007).
15. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 284(5418), 1318-1322 (1999).
16. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet 358(9276), 135-138 (2001).
17. Otto M. Staphylococcal biofilms. Curr. Top. Microbiol. Immunol. 322, 207-228 (2008).
18. Mack D, Fischer W, Krokotsch A et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178(1), 175-183 (1996).
19. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67(10), 5427-5433 (1999).
20. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20(5), 1083-1091 (1996).
21. Gerke C, Kraft A, Sussmuth R, Schweitzer O, Gotz F. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J. Biol. Chem. 273(29), 18586-18593 (1998).
22. Vuong C, Kocianova S, Voyich JM et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem. 279(52), 54881-54886 (2004).
23. Otto M. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu. Rev. Med. 64, 175-188 (2013).
24. O'Riordan K, Lee JC. Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev. 17(1), 218-234 (2004).
25. Nilsson IM, Lee JC, Bremell T, Ryden C, Tarkowski A. The role of staphylococcal polysaccharide microcapsule expression in septicemia and septic arthritis. Infect. Immun. 65(10), 4216-4221 (1997).
26. Boyle-Vavra S, Li X, Alam MT et al. USA300 and USA500 clonal lineages of Staphylococcus aureus do not produce a capsular polysaccharide due to conserved mutations in the cap5 locus. MBio 6(2), (2015).
27. Foster TJ, Geoghegan JA, Ganesh VK, Hook M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 12(1), 49-62 (2014).
28. Beenken KE, Dunman PM, Mcaleese F et al. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 186(14), 4665-4684 (2004).
29. Resch A, Leicht S, Saric M et al. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6(6), 1867-1877 (2006).
30. Yao Y, Sturdevant DE, Otto M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J. Infect. Dis. 191(2), 289-298 (2005).
31. Novick RP, Geisinger E. Quorum sensing in staphylococci. Annu. Rev. Genet. 42, 541-564 (2008).
32. Cheung AL, Nishina KA, Trotonda MP, Tamber S. The SarA protein family of Staphylococcus aureus. Int. J. Biochem. Cell. Biol. 40(3), 355-361 (2008).
33. Hecker M, Reder A, Fuchs S, Pagels M, Engelmann S. Physiological proteomics and stress/starvation responses in Bacillus subtilis and Staphylococcus aureus. Res. Microbiol. 160(4), 245-258 (2009).
34. Fournier B, Klier A, Rapoport G. The two-component system ArlS-ArlR is a regulator of virulence gene expression in Staphylococcus aureus . Mol. Microbiol. 41(1), 247-261 (2001).
35. Pragman AA, Yarwood JM, Tripp TJ, Schlievert PM. Characterization of virulence factor regulation by SrrAB, a two-component system in Staphylococcus aureus. J. Bacteriol. 186(8), 2430-2438 (2004).
36. Cheung AL, Bayer MG, Heinrichs JH. sar Genetic determinants necessary for transcription of RNAII and RNAIII in the agr locus of Staphylococcus aureus. J. Bacteriol. 179(12), 3963-3971 (1997).
37. Ziebandt AK, Weber H, Rudolph J et al. Extracellular proteins of Staphylococcus aureus and the role of SarA and sigma B. Proteomics 1(4), 480-493 (2001).
38. Nicholas RO, Li T, Mcdevitt D et al. Isolation and characterization of a sigB deletion mutant of Staphylococcus aureus. Infect. Immun. 67(7), 3667-3669 (1999).
39. Deora R, Tseng T, Misra TK. Alternative transcription factor sigmaSB of Staphylococcus aureus: characterization and role in transcription of the global regulatory locus sar. J. Bacteriol. 179(20), 6355-6359 (1997).
40. Yarwood JM, Mccormick JK, Schlievert PM. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J. Bacteriol. 183(4), 1113-1123 (2001).
41. Fournier B, Hooper DC. A new twocomponent regulatory system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J. Bacteriol. 182(14), 3955-3964 (2000).
42. Fuchs S, Pane-Farre J, Kohler C, Hecker M, Engelmann S. Anaerobic gene expression in Staphylococcus aureus. J. Bacteriol. 189(11), 4275-4289 (2007).
43. Yarwood JM, Mccormick JK, Paustian ML, Kapur V, Schlievert PM. Repression of the Staphylococcus aureus accessory gene regulator in serum and in vivo. J. Bacteriol. 184(4), 1095-1101 (2002).
44. Ulrich M, Bastian M, Cramton SE et al. The staphylococcal respiratory response regulator SrrAB induces ica gene transcription and polysaccharide intercellular adhesin expression, protecting Staphylococcus aureus from neutrophil killing under anaerobic growth conditions. Mol. Microbiol. 65(5), 1276-1287 (2007).
45. Park MK, Myers RA, Marzella L. Oxygen tensions and infections: modulation of microbial growth, activity of antimicrobial agents, and immunologic responses. Clin. Infect. Dis. 14(3), 720-740 (1992).
46. Lund-Olesen K. Oxygen tension in synovial fluids. Arthritis Rheum. 13(6), 769-776 (1970).
47. Weinrick B, Dunman PM, Mcaleese F et al. Effect of mild acid on gene expression in Staphylococcus aureus. J. Bacteriol. 186(24), 8407-8423 (2004).
48. Chan PF, Foster SJ. The role of environmental factors in the regulation of virulencedeterminant expression in Staphylococcus aureus 8325-4. Microbiology 144(Pt 9), 2469-2479 (1998).
49. Regassa LB, Novick RP, Betley MJ. Glucose and nonmaintained pH decrease expression of the accessory gene regulator (agr) in Staphylococcus aureus. Infect. Immun. 60(8), 3381-3388 (1992).
50. Regassa LB, Betley MJ. High sodium chloride concentrations inhibit staphylococcal enterotoxin C gene (sec) expression at the level of sec mRNA. Infect. Immun. 61, 1581-1585 (1993).
51. Genigeorgis C, Sadler WW. Effect of sodium chloride and pH on enterotoxin B production. J. Bacteriol. 92(5), 1383-1387 (1966).
52. Sheehan BJ, Foster TJ, Dorman CJ, Park S, Stewart GS. Osmotic and growth-phase dependent regulation of the eta gene of Staphylococcus aureus: a role for DNA supercoiling. Mol. Gen. Genet. 232(1), 49-57 (1992).
53. Mekalanos JJ. Environmental signals controlling expression of virulence determinants in bacteria. J. Bacteriol. 174(1), 1-7 (1992).
54. Reeves MW. Effect of trace metals on the synthesis of toxic shock syndrome toxin 1. Rev. Infect. Dis. 11(Suppl. 1), S145-S149; discussion S149-S150 (1989).
55. Allard M, Moisan H, Brouillette É et al. Transcriptional modulation of some Staphylococcus aureus iron-regulated genes during growth in vitro and in a tissue cage model in vivo. Microbes Infect. 8(7), 1679-1690 (2006).
56. Harder J, Schroder JM. Antimicrobial peptides in human skin. Chem. Immunol. Allergy 86, 22-41 (2005).
57. Herbert S, Bera A, Nerz C et al. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3(7), e102 (2007).
58. Li M, Lai Y, Villaruz AE, Cha DJ, Sturdevant DE, Otto M. Gram-positive three-component antimicrobial peptide-sensing system. Proc. Natl Acad. Sci. USA 104(22), 9469-9474 (2007).
59. Li M, Cha DJ, Lai Y, Villaruz AE, Sturdevant DE, Otto M. The antimicrobial peptidesensing system aps of Staphylococcus aureus. Mol. Microbiol. 66(5), 1136-1147 (2007).
60. Pietiainen M, Francois P, Hyyrylainen HL et al. 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 (2009).
61. Peschel A, Jack RW, Otto M et al. 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(9), 1067-1076 (2001).
62. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Gotz F. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274(13), 8405-8410 (1999).
63. Falord M, Karimova G, Hiron A, Msadek T. GraXSR proteins interact with the VraFG ABC transporter to form a five-component system required for cationic antimicrobial peptide sensing and resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 56(2), 1047-1058 (2012).
64. Chang W, Small DA, Toghrol F, Bentley WE. Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide. J. Bacteriol. 188(4), 1648-1659 (2006).
65. Stevens DL, Ma Y, Salmi DB, Mcindoo E, Wallace RJ, Bryant AE. Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillinresistant Staphylococcus aureus. J. Infect. Dis. 195(2), 202-211 (2007).
66. Joo HS, Chan JL, Cheung GY, Otto M. Subinhibitory concentrations of protein synthesis-inhibiting antibiotics promote increased expression of the agr virulence regulator and production of phenol-soluble modulin cytolysins in community-associated methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 54(11), 4942-4944 (2010).
67. Ohlsen K, Ziebuhr W, Koller KP, Hell W, Wichelhaus TA, Hacker J. Effects of subinhibitory concentrations of antibiotics on alpha-toxin (hla) gene expression of methicillin-sensitive and methicillin-resistant Staphylococcus aureusisolates. Antimicrob. Agents Chemother. 42(11), 2817-2823 (1998).
68. Foster TJ, Hook M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6(12), 484-488 (1998).
69. Cheung GY, Wang R, Khan BA, Sturdevant DE, Otto M. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 79(5), 1927-1935 (2011).
70. Otto M. Staphylococcus epidermidis-the 'accidental' pathogen. Nat. Rev. Microbiol. 7(8), 555-567 (2009).
71. Otto M. Virulence factors of the coagulasenegative staphylococci. Front. Biosci. 9, 841-863 (2004).
72. Wertheim HF, Melles DC, Vos MC et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 5(12), 751-762 (2005).
73. Yang ES, Tan J, Eells S, Rieg G, Tagudar G, Miller LG. Body site colonization in patients with community-associated methicillinresistant Staphylococcus aureus and other types of S. aureus skin infections. Clin. Microbiol. Infect. 16(5), 425-431 (2010).
74. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375(9725), 1557-1568 (2010).
75. Lowy FD. Staphylococcus aureus infections. N. Engl. J. Med. 339(8), 520-532 (1998).
76. Grice EA, Segre JA. The skin microbiome. Nat. Rev. Microbiol. 9(4), 244-253 (2011).
77. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 326(5960), 1694-1697 (2009).
78. Chiller K, Selkin BA, Murakawa GJ. Skin microflora and bacterial infections of the skin. J. Investig. Dermatol. Symp. Proc. 6(3), 170-174 (2001).
79. Garzoni C, Kelley WL. Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol. 17(2), 59-65 (2009).
80. Von Eiff C, Becker K, Metze D et al. Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with darier's disease. Clin. Infect. Dis. 32(11), 1643-1647 (2001).
81. Rogers DE, Tompsett R. The survival of staphylococci within human leukocytes. J. Exp. Med. 95(2), 209-230 (1952).
82. Bayles KW, Wesson CA, Liou LE, Fox LK, Bohach GA, Trumble WR. Intracellular Staphylococcus aureusescapes the endosome and induces apoptosis in epithelial cells. Infect. Immun. 66(1), 336-342 (1998).
83. Garzoni C, Francois P, Huyghe A et al. A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 8, 171 (2007).
84. Grosz M, Kolter J, Paprotka K et al. Cytoplasmic replication of Staphylococcus aureus upon phagosomal escape triggered by phenol-soluble modulin alpha. Cell. Microbiol. 16(4), 451-465 (2014).
85. Surewaard BG, De Haas CJ, Vervoort F et al. Staphylococcal alpha-phenol soluble modulins contribute to neutrophil lysis after phagocytosis. Cell. Microbiol. 15(8), 1427-1437 (2013).
86. Voyich JM, Braughton KR, Sturdevant DE et al. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175(6), 3907-3919 (2005).
87. Loughman JA, Fritz SA, Storch GA, Hunstad DA. Virulence gene expression in human community-acquired Staphylococcus aureus infection. J. Infect. Dis. 199(3), 294-301 (2009).
88. Malachowa N, Kobayashi SD, Sturdevant DE, Scott DP, DeLeo FR. Insights into the Staphylococcus aureus-host interface: global changes in host and pathogen gene expression in a rabbit skin infection model. PLoS ONE 10(2), e0117713 (2015).
89. Date SV, Modrusan Z, Lawrence M et al. Global gene expression of methicillin-resistant Staphylococcus aureus USA300 during human and mouse infection. J. Infect. Dis. 209(10), 1542-1550 (2014).
90. Weidenmaier C, Kokai-Kun JF, Kristian SA et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10(3), 243-245 (2004).
91. Weidenmaier C, Kokai-Kun JF, Kulauzovic E et al. Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int. J. Med. Microbiol. 298(5-6), 505-513 (2008).
92. Kokai-Kun JF, Walsh SM, Chanturiya T, Mond JJ. Lysostaphin cream eradicates Staphylococcus aureus nasal colonization in a cotton rat model. Antimicrob. Agents Chemother. 47(5), 1589-1597 (2003).
93. Kiser KB, Cantey-Kiser JM, Lee JC. Development and characterization of a Staphylococcus aureusnasal colonization model in mice. Infect. Immun. 67(10), 5001-5006 (1999).
94. Burian M, Wolz C, Goerke C. Regulatory adaptation of Staphylococcus aureus during nasal colonization of humans. PLoS ONE 5(4), e10040 (2010).
95. Von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N. Engl. J. Med. 344(1), 11-16 (2001).
96. Rao N, Jacobs S, Joyce L. Cost-effective eradication of an outbreak of methicillinresistant Staphylococcus aureus in a community teaching hospital. Infect. Control Hosp. Epidemiol. 9(6), 255-260 (1988).
97. Hacek DM, Paule SM, Thomson RB Jr., Robicsek A, Peterson LR. Implementation of a universal admission surveillance and decolonization program for methicillinresistant Staphylococcus aureus (MRSA) reduces the number of MRSA and total number of S. aureus isolates reported by the clinical laboratory. J. Clin. Microbiol. 47(11), 3749-3752 (2009).
98. Ammerlaan HS, Kluytmans JA, Wertheim HF, Nouwen JL, Bonten MJ. Eradication of methicillin-resistant Staphylococcus aureus carriage: a systematic review. Clin. Infect. Dis. 48(7), 922-930 (2009).
99. Bode LG, Kluytmans JA, Wertheim HF et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N. Engl. J. Med. 362(1), 9-17 (2010).
100. Van Rijen MM, Bonten M, Wenzel RP, Kluytmans JA. Intranasal mupirocin for reduction of Staphylococcus aureus infections in surgical patients with nasal carriage: a systematic review. J. Antimicrob. Chemother. 61(2), 254-261 (2008).
101. Krismer B, Peschel A. Does Staphylococcus aureus nasal colonization involve biofilm formation Future Microbiol. 6(5), 489-493 (2011).
102. Rosenzweig SD, Holland SM. Recent insights into the pathobiology of innate immune deficiencies. Curr. Allergy Asthma Rep. 11(5), 369-377 (2011).
103. Von Bernuth H, Picard C, Jin Z et al. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321(5889), 691-696 (2008).
104. Lee MH, Arrecubieta C, Martin FJ, Prince A, Borczuk AC, Lowy FD. A postinfluenza model of Staphylococcus aureus pneumonia. J. Infect. Dis. 201(4), 508-515 (2010).
105. Chaffin DO, Taylor D, Skerrett SJ, Rubens CE. Changes in the Staphylococcus aureus transcriptome during early adaptation to the lung. PLoS ONE 7(8), e41329 (2012).
106. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28(3), 603-661 (2015).
107. Miro JM, Anguera I, Cabell CH et al. Staphylococcus aureus native valve infective endocarditis: report of 566 episodes from the International Collaboration on Endocarditis Merged Database. Clin. Infect. Dis. 41(4), 507-514 (2005).
108. Shrestha NK, Jue J, Hussain ST et al. Injection drug use and outcomes after surgical intervention for infective endocarditis. Ann. Thorac. Surg. (2015).
109. Xiong YQ, Willard J, Yeaman MR, Cheung AL, Bayer AS. Regulation of Staphylococcus aureus alpha-toxin gene (hla) expression by agr sarA and sae in vitro and in experimental infective endocarditis. J. Infect. Dis. 194(9), 1267-1275 (2006).
110. Hanses F, Roux C, Dunman PM, Salzberger B, Lee JC. Staphylococcus aureus gene expression in a rat model of infective endocarditis. Genome Med. 6(10), 93 (2014).
111. Malachowa N, Whitney AR, Kobayashi SD et al. Global changes in Staphylococcus aureus gene expression in human blood. PLoS ONE 6(4), e18617 (2011).
112. Den Reijer PM, Lemmens-Den Toom N, Kant S et al. Characterization of the humoral immune response during Staphylococcus aureus bacteremia and global gene expression by Staphylococcus aureus in human blood. PLoS ONE 8(1), e53391 (2013).
113. Dastgheyb SS, Villaruz AE, Le KY et al. Role of Phenol-Soluble Modulins in Formation of Staphylococcus aureus Biofilms in Synovial Fluid. Infect. Immun. 83(7), 2966-2975 (2015).
114. Wang R, Khan BA, Cheung GY et al. Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J. Clin. Invest. 121(1), 238-248 (2011).
115. Periasamy S, Joo HS, Duong AC et al. Staphylococcus aureus biofilms develop their characteristic structure. Proc. Natl Acad. Sci. USA 109(4), 1281-1286 (2012).
116. Fowler VG Jr., Sakoulas G, McIntyre LM et al. Persistent bacteremia due to methicillinresistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. J. Infect. Dis. 190(6), 1140-1149 (2004).
117. Oogai Y, Matsuo M, Hashimoto M, Kato F, Sugai M, Komatsuzawa H. Expression of virulence factors by Staphylococcus aureus grown in serum. Appl. Environ. Microbiol. 77(22), 8097-8105 (2011).
118. Shirtliff ME, Mader JT. Acute septic arthritis. Clin. Microbiol. Rev. 15(4), 527-544 (2002).
119. Fass RJ. Treatment of osteomyelitis and septic arthritis with cefazolin. Antimicrob. Agents Chemother. 13(3), 405-411 (1978).
120. Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol. Med. Microbiol. 65(2), 158-168 (2012).
121. Hudson MC, Ramp WK, Nicholson NC, Williams AS, Nousiainen MT. Internalization of Staphylococcus aureus by cultured osteoblasts. Microb. Pathog. 19(6), 409-419 (1995).
122. Szafranska AK, Oxley AP, Chaves-Moreno D et al. High-resolution transcriptomic analysis of the adaptive response of Staphylococcus aureus during acute and chronic phases of osteomyelitis. MBio 5(6), e01775-14 (2014).
123. Parvizi J, Ghanem E, Sharkey P, Aggarwal A, Burnett RS, Barrack RL. Diagnosis of infected total knee: findings of a multicenter database. Clin. Orthop. Relat. Res. 466(11), 2628-2633 (2008).
124. Dastgheyb S, Parvizi J, Shapiro IM, Hickok NJ, Otto M. Effect of biofilms on recalcitrance of staphylococcal joint infection to antibiotic treatment. J. Infect. Dis. 211(4), 641-650 (2015).
125. Naesens R, Ronsyn M, Druwe P, Denis O, Ieven M, Jeurissen A. Central nervous system invasion by community-acquired meticillinresistant Staphylococcus aureus. J. Med. Microbiol. 58(Pt 9), 1247-1251 (2009).
126. Fong IW. Staphylococcal central nervous system infections treated with cloxacillin. J. Antimicrob. Chemother. 12(6), 607-612 (1983).
127. Jordan PA, Iravani A, Richard GA, Baer H. Urinary tract infection caused by Staphylococcus saprophyticus. J. Infect. Dis. 142(4), 510-515 (1980).
128. Raz R, Colodner R, Kunin CM. Who are you-Staphylococcus saprophyticus Clin. Infect. Dis. 40(6), 896-898 (2005).
129. Dobrindt U. [Virulence factors of uropathogens]. Urologe A 49(5), 598-605 (2010).
130. Gad GF, El-Feky MA, El-Rehewy MS, Hassan MA, Abolella H, El-Baky RM. Detection of icaA icaD genes and biofilm production by Staphylococcus aureus and Staphylococcus epidermidis isolated from urinary tract catheterized patients. J. Infect. Dev. Ctries 3(5), 342-351 (2009).
131. Kaye D. Antibacterial activity of human urine. J. Clin. Invest. 47(10), 2374-2390 (1968).
132. Erdogan-Yildirim Z, Burian A, Manafi M, Zeitlinger M. Impact of pH on bacterial growth and activity of recent fluoroquinolones in pooled urine. Res. Microbiol. 162(3), 249-252 (2011).
133. Veeh RH, Shirtliff ME, Petik JR et al. Detection of Staphylococcus aureus biofilm on tampons and menses components. J. Infect. Dis. 188(4), 519-530 (2003).
134. Kaur S, Prabha V. Infertility as a consequence of spermagglutinating Staphylococcus aureus colonization in genital tract of female mice. PLoS ONE 7(12), e52325 (2012).
135. Ohri M, Prabha V. Isolation of a spermagglutinating factor from Staphylococcus aureus isolated from a woman with unexplained infertility. Fertil. Steril. 84(5), 1539-1541 (2005).
136. Ehlers C, Ivens UI, Moller ML, Senderovitz T, Serup J. Females have lower skin surface pH than men. A study on the surface of gender, forearm site variation, right/left difference and time of the day on the skin surface pH. Skin Res. Technol. 7(2), 90-94 (2001).
137. Raz R, Chazan B, Dan M. Cranberry juice and urinary tract infection. Clin. Infect. Dis. 38(10), 1413-1419 (2004).
138. England RJ, Homer JJ, Knight LC, Ell SR. Nasal pH measurement: a reliable and repeatable parameter. Clin. Otolaryngol. Allied Sci. 24(1), 67-68 (1999).
139. Wagner G, Ottesen B. Vaginal physiology during menstruation. Ann. Intern. Med. 96(6 Pt 2), 921-923 (1982).
140. Cheng DS, Rodriguez RM, Rogers J, Wagster M, Starnes DL, Light RW. Comparison of pleural fluid pH values obtained using blood gas machine, pH meter, and pH indicator strip. Chest 114(5), 1368-1372 (1998).
141. Robbie LA, Bennett B, Croll AM, Brown PA, Booth NA. Proteins of the fibrinolytic system in human thrombi. Thrombosis Haemostasis 75, 127-133 (1996).
142. Schultze HE, Heremans JF. Nature and metabolism of extracellular proteins. In: Molecular Biology Of Human Proteins With Special Reference To Plasma Proteins (Vol. 1). 473-477 (1966).
143. Tirumalai RS, Chan KC, Prieto DA, Issaq HJ, Conrads TP, Veenstra TD. Characterization of the low molecular weight human serum proteome. Mol. Cell. Proteomics 2(10), 1096-1103 (2003).
144. Charm SE, Kurland. GS. Blood Flow and Microcirculation.Wiley (1974).
145. Cokelet GR. The rheology of human blood. Biomechanics 72, 63-103 (1972).
146. Mcadow M, Kim HK, Dedent AC, Hendrickx AP, Schneewind O, Missiakas DM. Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLoS Pathog. 7(10), e1002307 (2011).
147. Jebens EH, Monk-Jones ME. On the viscosity and pH of synovial fluid and the pH of blood. J. Bone Joint Surg. Br. 41-B(2), 388-400 (1959).
148. Gibson DS, Rooney ME. The human synovial fluid proteome: a key factor in the pathology of joint disease. Proteomics Clin. Appl. 1(8), 889-899 (2007).
149. Ropes MW, Bennett GA, Bauer W. The origin and nature of normal synovial fluid. J. Clin. Invest. 18(3), 351-372 (1939).
150. Clarke B. Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol. 3(Suppl. 3), S131-S139 (2008).
151. Dastgheyb SS, Hammoud S, Ketonis C et al. Staphylococcal persistence due to biofilm formation in synovial fluid containing prophylactic cefazolin. Antimicrob. Agents Chemother. 59(4), 2122-2128 (2015).
152. Romeo MJ, Espina V, Lowenthal M, Espina BH, Iii EFP, Liotta LA. CSF proteome: a protein repository for potential biomarker identification. Expert Rev. Proteomics 2(1), 57-70 (2015).