Staphylococcus aureus adaptation to the host and persistence: Role of loss of capsular polysaccharide expression

Future Microbiology

Volumn 5, Issue 12, 2010, Pages 1823-1832

  Tuchscherr, Lorena ^a   Lffler, Bettina ^a   Buzzola, Fernanda R ^b,c   Sordelli, Daniel O ^b,c  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Capsule; Chronic; Evolution; Infection; Persistence; Staphylococcus aureus

Indexed keywords

ADHESIN; ALPHA HEMOLYSIN; ALPHA TOXIN; ANTIBIOTIC AGENT; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; CIPROFLOXACIN; MEMBRANE PROTEIN; PROTEINASE; SALICYLIC ACID; VIRULENCE FACTOR;

ACUTE DISEASE; AUTOPHAGY; BACTERIAL GENE; BACTERIAL VIRULENCE; CARBOHYDRATE SYNTHESIS; CELL INVASION; CHRONIC OSTEOMYELITIS; CHRONICITY; ENDOTHELIUM CELL; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; IC 50; NONHUMAN; OSTEOBLAST; OSTEOMYELITIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; SEROTYPE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ADAPTATION, BIOLOGICAL; BACTERIAL CAPSULES; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SPACE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 78650446312     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.10.147     Document Type: Review

References (82)

1. Que YA, Moreillon P: Staphylococcus aureus (including staphylococccal toxic shock). In: Principles and Practice of Infectious Diseases. Mandell GL, Bennet JE, Dolin R (Eds). Churchill-Livingstone-Elsevier, PA, USA (2010).
2. Gordon RJ, Lowy FD: Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46(Suppl. 5), S350-S359 (2008).
3. Kluytmans-Vandenbergh MF, Kluytmans JA: Community-acquired methicillin-resistant Staphylococcus aureus: current perspectives. Clin. Microbiol. Infect. 12(Suppl. 1), 9-15 (2006).
4. Deleo FR, Otto M, Kreiswirth BN, Chambers HF: Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375(9725), 1557-1568 (2010).
5. Kosowska-Shick K, Ednie LM, McGhee P et al.: Incidence and characteristics of vancomycin nonsusceptible strains of methicillin-resistant Staphylococcus aureus at Hershey Medical Center. Antimicrob. Agents Chemother. 52(12), 4510-4513 (2008).
6. Ikeda S, Hanaki H, Yanagisawa C et al.: Identification of the active component that induces vancomycin resistance in MRSA. J. Antibiot. (Tokyo) 63(9), 533-538 (2010).
7. van Belkum A, Melles DC, Nouwen J et al.: Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infect. Genet. Evol. 9(1), 32-47 (2009).
8. Herron-Olson L, Fitzgerald JR, Musser JM, Kapur V: Molecular correlates of host specialization in Staphylococcus aureus. PLoS One 2(10), E1120 (2007).
9. Alves PD, McCulloch JA, Even S et al.: Molecular characterisation of Staphylococcus aureus strains isolated from small and large ruminants reveals a host rather than tissue specificity. Vet. Microbiol. 137(1-2), 190-195 (2009).
10. Reinoso E, Bettera S, Frigerio C, DiRenzo M, Calzolari A, Bogni C: RAPD-PCR analysis of Staphylococcus aureus strains isolated from bovine and human hosts. Microbiol. Res. 159(3), 245-255 (2004).
11. Turner KM, Feil EJ: The secret life of the multilocus sequence type. Int. J. Antimicrob. Agents 29(2), 129-135 (2007).
12. Lattar SM, Tuchscherr LP, Caccuri RL et al.: Capsule expression and genotypic differences among Staphylococcus aureus isolates from patients with chronic or acute osteomyelitis. Infect. Immun. 77(5), 1968-1975 (2009).
13. Wright JA, Nair SP: Interaction of staphylococci with bone. Int. J. Med. Microbiol. 300(2-3), 193-204 (2009).
14. Lazzarini L, Mader JT, Calhoun JH: Osteomyelitis in long bones. J. Bone Joint Surg. Am. 86-A(10), 2305-2318 (2004).
15. Lew DP, Waldvogel FA: Osteomyelitis. Lancet 364(9431), 369-379 (2004).
16. Goerke C, Wolz C: Regulatory and genomic plasticity of Staphylococcus aureus during persistent colonization and infection. Int. J. Med. Microbiol. 294(2-3), 195-202 (2004).
17. Goerke C, Gressinger M, Endler K et al.: High phenotypic diversity in infecting but not in colonizing Staphylococcus aureus populations. Environ. Microbiol. 9(12), 3134-3142 (2007).
18. Lee CY, Lee JC: Staphylococcal capsule. In: Gram-positive pathogens. Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (Eds). ASM Press, Washington DC, USA, 456-463 (2006).
19. Hanssen AM, Ericson Sollid JU: SCCmec in staphylococci: genes on the move. FEMS Immunol. Med. Microbiol. 46(1), 8-20 (2006).
20. Cocchiaro JL, Gomez MI, Risley A, Solinga R, Sordelli DO, Lee JC: Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol. Microbiol. 59(3), 948-960 (2006).
21. Tuchscherr LP, Gomez MI, Buzzola FR, Calvinho LF, Lee JC, Sordelli DO: Characterization of a new variant of IS257 that has displaced the capsule genes within bovine isolates of Staphylococcus aureus. Infect. Immun. 75(11), 5483-5488 (2007).
22. Tuchscherr LP, Buzzola FR, Alvarez LP, Caccuri RL, Lee JC, Sordelli DO: Capsule-negative Staphylococcus aureus induces chronic experimental mastitis in mice. Infect. Immun. 73(12), 7932-7937 (2005).
23. Sordelli DO, Buzzola FR, Gomez MI et al.: Capsule expression by bovine isolates of Staphylococcus aureus from Argentina: genetic and epidemiologic analyses. J. Clin. Microbiol. 38(2), 846-850 (2000).
24. Werbick C, Becker K, Mellmann A et al.: Staphylococcal chromosomal cassette mec type I, spa type, and expression of Pls are determinants of reduced cellular invasiveness of methicillin-resistant Staphylococcus aureus isolates. J. Infect. Dis. 195(11), 1678-1685 (2007).
25. Sinha B, Herrmann M: Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus. Thromb. Haemost. 94(2), 266-277 (2005).
26. Sinha B, Fraunholz M: Staphylococcus aureus host cell invasion and post-invasion events. Int. J. Med. Microbiol. 300(2-3), 170-175 (2010).
27. Beaumont HJ, Gallie J, Kost C, Ferguson GC, Rainey PB: Experimental evolution of bet hedging. Nature 462(7269), 90-93 (2009).
28. Zautner AE, Krause M, Stropahl G et al.: Intracellular persisting Staphylococcus aureus is the major pathogen in recurrent tonsillitis. PLoS One 5(3), E9452 (2010).
29. Garzoni C, Kelley WL: Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol. 17(2), 59-65 (2009).
30. 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).
31. Sinha B FP, Nüsse O, Foti M et al.: Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin a5b1. Cell Microbiol. 1, 101-107 (1999).
32. Burian M, Rautenberg M, Kohler T et al.: Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J. Infect. Dis. 201(9), 1414-1421 (2010).
33. Cifrian E, Guidry AJ, OBrien CN, Marquardt WW: Effect of a-toxin and capsular exopolysaccharide on the adherence of Staphylococcus aureus to cultured teat, ductal and secretory mammary epithelial cells. Res. Vet. Sci. 58(1), 20-25 (1995).
34. Haagen IA, Heezius HC, Verkooyen RP, Verhoef J, Verbrugh HA: Adherence of peritonitis-causing staphylococci to human peritoneal mesothelial cell monolayers. J. Infect. Dis. 161(2), 266-273 (1990).
35. McKenney D, Pouliot KL, Wang Y et al.: Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284(5419), 1523-1527 (1999).
36. Pohlmann-Dietze P, Ulrich M, Kiser KB et al.: Adherence of Staphylococcus aureus to endothelial cells: influence of capsular polysaccharide, global regulator agr, and bacterial growth phase. Infect. Immun. 68(9), 4865-4871 (2000).
37. Risley AL, Loughman A, Cywes-Bentley C, Foster TJ, Lee JC: Capsular polysaccharide masks clumping factor A-mediated adherence of Staphylococcus aureus to fibrinogen and platelets. J. Infect. Dis. 196(6), 919-927 (2007).
38. Tuchscherr LP, Buzzola FR, Alvarez LP, Lee JC, Sordelli DO: Antibodies to capsular polysaccharide and clumping factor A prevent mastitis and the emergence of unencapsulated and small-colony variants of Staphylococcus aureus in mice. Infect. Immun. 76(12), 5738-5744 (2008).
39. Haslinger-Loffler B, Wagner B, Bruck M et al.: Staphylococcus aureus induces caspase-independent cell death in human peritoneal mesothelial cells. Kidney Int. 70(6), 1089-1098 (2006).
40. Mestre MB, Fader CM, Sola C, Colombo MI: A-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells. Autophagy 6(1), 110-125 (2010).
41. Haslinger-Loffler B, Kahl BC, Grundmeier M et al.: Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol. 7(8), 1087-1097 (2005).
42. Grundmeier M, Tuchscherr L, Bruck M et al.: Staphylococcal strains vary greatly in their ability to induce an inflammatory response in endothelial cells. J. Infect. Dis. 201(6), 871-880 (2010).
43. Lam TT, Giese B, Chikkaballi D et al.: Phagolysosomal integrity is generally maintained after Staphylococcus aureus invasion of nonprofessional phagocytes but is modulated by strain 6850. Infect. Immun. 78(8), 3392-3403 (2010).
44. Koziel J, Maciag-Gudowska A, Mikolajczyk T et al.: Phagocytosis of Staphylococcus aureus by macrophages exerts cytoprotective effects manifested by the upregulation of antiapoptotic factors. PLoS One 4(4), E5210 (2009).
45. Kubica M, Guzik K, Koziel J et al.: A potential new pathway for Staphylococcus aureus dissemination: the silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PLoS One 3(1), E1409 (2008).
46. Tuchscherr L, Heitmann V, Hussain M et al.: Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. J. Infect. Dis. 202(7), 1031-1040 (2010).
47. Vesga O, Groeschel MC, Otten MF, Brar DW, Vann JM, Proctor RA: Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J. Infect. Dis. 173(3), 739-742 (1996).
48. Proctor RA, von Eiff C, Kahl BC et al.: Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol. 4(4), 295-305 (2006).
49. Goerke C, Wolz C: Adaptation of Staphylococcus aureus to the cystic fibrosis lung. Int. J. Med. Microbiol. DOI 10.1016/j. ijmm.2010.08.003 (2010) (Epub ahead of print).
50. ORiordan K, Lee JC: Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev. 17(1), 218-234 (2004).
51. Schaffer AC, Lee JC: Vaccination and passive immunisation against Staphylococcus aureus. Int. J. Antimicrob. Agents 32(Suppl. 1), S71-S78 (2008).
52. Novick RP, Geisinger E: Quorum sensing in staphylococci. Annual Rev. Genet. 42, 541-564 (2008).
53. Buzzola FR, Alvarez LP, Tuchscherr LP et al.: Differential abilities of capsulated and noncapsulated Staphylococcus aureus isolates from diverse agr groups to invade mammary epithelial cells. Infect. Immun. 75(2), 886-891 (2007).
54. Goerke C, Fluckiger U, Steinhuber A et al.: Role of Staphylococcus aureus global regulators sae and sB in virulence gene expression during device-related infection. Infect. Immun. 73(6), 3415-3421 (2005).
55. Adhikari RP, Novick RP: Regulatory organization of the staphylococcal sae locus. Microbiology 154(Pt 3), 949-959 (2008).
56. Geiger T, Goerke C, Mainiero M, Kraus D, Wolz C: The virulence regulator Sae of Staphylococcus aureus: promoter activities and response to phagocytosis-related signals. J. Bacteriol. 190(10), 3419-3428 (2008).
57. Mainiero M, Goerke C, Geiger T, Gonser C, Herbert S, Wolz C: Differential target gene activation by the Staphylococcus aureus two-component system saeRS. J. Bacteriol. 192(3), 613-623 (2010).
58. Rogasch K, Ruhmling V, Pane-Farre J et al.: Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J. Bacteriol. 188(22), 7742-7758 (2006).
59. 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).
60. Ballal A, Ray B, Manna AC: sarZ, a sarA family gene, is transcriptionally activated by MgrA and is involved in the regulation of genes encoding exoproteins in Staphylococcus aureus. J. Bacteriol. 191(5), 1656-1665 (2009).
61. Kaatz GW, Thyagarajan RV, Seo SM: Effect of promoter region mutations and mgrA overexpression on transcription of norA, which encodes a Staphylococcus aureus multidrug efflux transporter. Antimicrob. Agents Chemother. 49(1), 161-169 (2005).
62. Truong-Bolduc QC, Strahilevitz J, Hooper DC: NorC, a new efflux pump regulated by MgrA of Staphylococcus aureus. Antimicrob. Agents Chemother. 50(3), 1104-1107 (2006).
63. Chen Z, Luong TT, Lee CY: The sbcDC locus mediates repression of type 5 capsule production as part of the SOS response in Staphylococcus aureus. J. Bacteriol. 189(20), 7343-7350 (2007).
64. Luong TT, Dunman PM, Murphy E, Projan SJ, Lee CY: Transcription profiling of the mgrA regulon in Staphylococcus aureus. J. Bacteriol. 188(5), 1899-1910 (2006).
65. Meier S, Goerke C, Wolz C et al.: sB and the sB-dependent arlRS and yabJ-spoVG loci affect capsule formation in Staphylococcus aureus. Infect. Immun. 75(9), 4562-4571 (2007).
66. Seidl K, Stucki M, Ruegg M et al.: Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob. Agents Chemother. 50(4), 1183-1194 (2006).
67. Zhao L, Xue T, Shang F, Sun H, Sun B: Staphylococcus aureus AI-2 quorum sensing associates with the kdpDE two-component system to regulate capsular polysaccharide synthesis and virulence. Infect. Immun. 78(8), 3506-3515 (2010).
68. Manna AC, Cheung AL: Expression of SarX, a negative regulator of agr and exoprotein synthesis, is activated by MgrA in Staphylococcus aureus. J. Bacteriol. 188(12), 4288-4299 (2006).
69. Kiser KB, Cantey-Kiser JM, Lee JC: Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect. Immun. 67(10), 5001-5006 (1999).
70. Arbeit RD, Nelles MJ: Capsular polysaccharide antigenemia in rats with experimental endocarditis due to Staphylococcus aureus. J. Infect. Dis. 155(2), 242-246 (1987).
71. Lee JC, Takeda S, Livolsi PJ, Paoletti LC: Effects of in vitro and in vivo growth conditions on expression of type 8 capsular polysaccharide by Staphylococcus aureus. Infect. Immun. 61(5), 1853-1858 (1993).
72. Arbeit RD, Dunn RM: Expression of capsular polysaccharide during experimental focal infection with Staphylococcus aureus. J. Infect. Dis. 156(6), 947-952 (1987).
73. Hensen SM, Pavicic MJ, Lohuis JA, de Hoog JA, Poutrel B: Location of Staphylococcus aureus within the experimentally infected bovine udder and the expression of capsular polysaccharide type 5 in situ. J. Dairy Sci. 83(9), 1966-1975 (2000).
74. Herbert S, Worlitzsch D, Dassy B et al.: Regulation of Staphylococcus aureus capsular polysaccharide type 5: CO2 inhibition in vitro and in vivo. J. Infect. Dis. 176(2), 431-438 (1997). (Pubitemid 27328766)
75. Sadykov MR, Mattes TA, Luong TT et al.: Tricarboxylic acid cycle-dependent synthesis of Staphylococcus aureus type 5 and 8 capsular polysaccharides. J. Bacteriol. 192(5), 1459-1462 (2010).
76. Somerville GA, Proctor RA: At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci. Microbiol. Mol. Biol. Rev. 73(2), 233-248 (2009).
77. Pohl K, Francois P, Stenz L et al.: CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J. Bacteriol. 191(9), 2953-2963 (2009).
78. Majerczyk CD, Dunman PM, Luong TT et al.: Direct targets of CodY in Staphylococcus aureus. J. Bacteriol. 192(11), 2861-2877 (2010).
79. Cirz RT, Jones MB, Gingles NA et al.: Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J. Bacteriol. 189(2), 531-539 (2007).
80. Kuroda H, Kuroda M, Cui L, Hiramatsu K: Subinhibitory concentrations of b-lactam induce haemolytic activity in Staphylococcus aureus through the SaeRS two-component system. FEMS Microbiol. Lett. 268(1), 98-105 (2007).
81. Palma M, Bayer A, Kupferwasser LI, Joska T, Yeaman MR, Cheung A: Salicylic acid activates s factor B by rsbU-dependent and -independent mechanisms. J. Bacteriol. 188(16), 5896-5903 (2006).
82. Alvarez LP, Barbagelata MS, Gordiola M, Cheung AL, Sordelli DO, Buzzola FR: Salicylic acid diminishes Staphylococcus aureus capsular polysaccharide type 5 expression. Infect. Immun. 78(3), 1339-1344 (2010).