A potential new pathway for Staphylococcus aureus dissemination: The silent survival of S. aureus phagocytosed by human monocyte-derived macrophages

PLoS ONE

Volumn 3, Issue 1, 2008, Pages

  Kubica, Malgorzata ^a   Guzik, Krzysztof ^a   Koziel, Joanna ^a   Zarebski, Miroslaw ^a   Richter, Walter ^b   Gajkowska, Barbara ^c   Golda, Anna ^a   Maciag Gudowska, Agnieszka ^a   Brix, Klaudia ^d   Shaw, Les ^e   Foster, Timothy ^f   Potempa, Jan ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^d JACOBS UNIVERSITY BREMEN   (Germany)

^e UNIVERSITY OF SOUTH FLORIDA   (United States)

^f TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

AUREOLYSIN PROTEIN; BACTERIAL TOXIN; GAMMA INTERFERON; METALLOPROTEINASE; PROTEIN A; PROTEIN AGR; REGULATOR PROTEIN; SIGMA FACTOR; SMAD ANCHOR FOR RECEPTOR ACTIVATION; SORTASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL INTERACTION; CELL MOTILITY; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; CYTOLYSIS; CYTOPLASM; DISEASE COURSE; HUMAN; HUMAN CELL; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MAMMAL CELL; MICROBIAL ACTIVITY; MONOCYTE; NONHUMAN; PATHOPHYSIOLOGY; PHAGOCYTOSIS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; IMMUNOLOGY; MACROPHAGE; MICROBIOLOGY; PHYSIOLOGY; SERUM BACTERICIDAL ACTIVITY;

MAMMALIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

BLOOD BACTERICIDAL ACTIVITY; HUMANS; MACROPHAGES; MONOCYTES; PHAGOCYTOSIS; STAPHYLOCOCCUS AUREUS;

EID: 39049169762     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001409     Document Type: Article

References (87)

1. Archer GL (1998) Staphylococcus aureus: A well-armed pathogen. Clin Infect Dis 26: 1179-1181.
2. Lowy FD (1998) Staphylacoccus aureus infections. New Engl J Med 339: 520-532.
3. Zetola N, Francis JS, Nuermberger EL, Bishai WR (2005) Community-acquired meticillin-resistant: an emerging threat. Lancet Infect Dis 5: 275-286.
4. Foster TJ, Hook M (1998) Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6: 484-488.
5. Foster TJ (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3: 948-958.
6. Lindsay JA, Holden MT (2004) Staphylococcus aureus: superbug, super genome? Trends Microbiol 12: 378-385.
7. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ (2004) Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureu. FEMS Immunol Med Microbiol 40: 1-9.
8. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48: 1429-1449.
9. Bischoff M, Entenza JM, Giachino P (2001) Influence of a functional sigB operon on the global regulators sar and agr in Staphylococcus aureus. J Bacteriol 183: 5171-5179.
10. Bronner S, Monteil H, Prevost G (2003) Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev 28: 183-200.
11. Abdelnour A, Arvidson S, Bremell T, Ryden C, Tarkowski A (1993) The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect Immun 61: 3879-3885.
12. Booth MC, Cheung AL, Hatter KL, Jett BD, Callegan MC, et al. (1997) Staphylococcal accessory regulator (sar in conjunction with agr contributes to Staphylococcus aureus virulence in endophthalmitis. Infect Immun 65: 1550-1556.
13. Cheung AL, Eberhardt KJ, Chung E, Yeaman MR, Sullam PM, et al. (1994) Diminished virulence of a sar-agr- mutant of Staphylococcus aureus in the rabbit model of endocarditis. J Clin Invest 94: 1815-1822.
14. Clement S, Vaudaux P, Francois P, Schrenzel J, Huggler E, et al. (2005) Evidence of an intracellular reservoir in die nasal mucosa of patients with recurrent Staphylococcus aureus rhinosinusitis. J Infect Dis 192: 1023-1028.
15. Bayles KW, Wesson CA, Liou LE, Fox LK, Bohach GA, et al. (1998) Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect Immun 66: 336-342.
16. Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, et al. (2000) Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell bcta-1-integrins. Eur J Cell Biol 79: 672-679.
17. Hess DJ, Henry-Stanley MJ, Erickson EA, Wells CL (2003) Intraceltular survival of Staphylococcus aureus within cultured enterocytes. J Surg Res 114: 42-49.
18. Menzies BE, Kourteva I (1998) Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect Immun 66. 5994-5998.
19. Nair SP, Bischoff M, Senn MM, Berger-Bachi B (2003) The sigma B regulon influences internalization of Staphylococcus aureus by osteoblasts. Infect Immun 71: 4167-4170.
20. Nuzzo I, Sanges MR, Folgore A, Carratelli CR (2000) Apoptosis of human keratinocytes after bacterial invasion. FEMS Immunol Med Microbiol 27: 235-240.
21. Peacock SJ, Foster TJ, Cameron BJ, Berendt AR (1999) Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial rells. Microbiology 145: 3477-3486.
22. Dziewanowska K, Patti JM, Deobald CF, Bayles KW, Trumble WR, et al. (1999) Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect Immun 67: 4673-4678.
23. Sinha B, Francois PP, Nusse O, Foti M, Hartford OM, et al. (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1: 101-117.
24. Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, et al. (2005) Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci 118: 2189-200.
25. Fowler T, Johansson S, Wary KK, Hook M (2003) Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus. Cell Microbiol 5: 417-426.
26. Lowy FD, Fant J, Higgins LL, Ogawa SK, Hatcher VB (1988) Staphylacoccus aureus-human endothelial cell interactions. J Ultrastruct Mol Struct Res 98: 137-146.
27. Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, et al. (2007) Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem 282: 2695-2706.
28. Jones D, Walev I, Berger T, Liebetrau M, Palmer M, et al. (1994) Novel path to apoptosis: small transmembrane pores created by staphylococcal alpha-toxin in T lymphocytes evoke internucleosomal DNA degradation. Infect Immun 62: 1304-1312.
29. de Silva MC, Zahm JM, Gras D, Bajolet O, Abely M, et al. (2004) Dynamic interaction between airway epithelial cells and Staphylococcus aureus. Am J Physiol Lung Cell Mol Physiol 287: L543-L551.
30. Haslinger B, Strangfeld K, Peters G, Schulze-Osthoff K, Sinha B (2003) Staphylococcus aureus alpha-toxin induces apoptosis in peripheral blood mononuclear cells: role of endogenous tumour necrosis factor-alpha and the mitochondrial death pathway. Cell Microbiol 5: 729-741.
31. Esen M, Schreiner B, Jendrossek V, Lang F, Fassbender K, et al. (2001) Mechanism of Staphylococcus aureus induced apoptosis of human endothelial cells. Apoptosis 6: 431-439.
32. Haslinger-Loffler B, Kahl BC, Grundmeier M, Strangfeld K, Wagner B, et al. (2005) Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol 7: 1087-1097.
33. Wesson CA, Liou LE, Todd KM, Bohach GA, Trimble WR, et al. (1998) Staphylococcus aureus Agr and Sar global regulators influence internalization and induction of apoptosis. Infect Immum 66: 5238-5243.
34. Amer AO, Swanson MS (2002) A phagosome of one's own: a microbial guide to life in the macrophage. Curr Opin Microbiol 5: 56-61.
35. Staab 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.
36. Kapral F, Shayegani F (1959) Intracellular survival of staphylococci. J Exp Med 110: 123-138.
37. Melly M, Thomison J, Rogers D (1960) Fate of staphylococci with human leukocytes. J Exp Med 112: 1121-1130.
38. Rogers DE, Tompsett R (1952) The survival of staphylococci within human leukocytes. J Exp Med 95: 209-230.
39. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, et al. (2005) Insights into mechanism used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
40. Gresham HD, Lowrance JH, Caver TE, Wilson BS, Cheung AL, et al. (2000) Survival of Staphylococcus aureus inside neutrophils contributes to infection. J Immunol 164: 3713-3722.
41. Savill J, Haslett C (1994) Fate of Neutrophils. In: Hellewell PG, Williams TJ, eds (1994) Immunopharmacology of Neutrophils Academic Press Inc.. pp 295-314.
42. Bellingan GJ, Caldwell H, Howie SEM, Dransfield I, Haslett C (1996) In vivo fate of the inflammatory macrophageduring the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes, J Immumol 157: 2577-2585.
43. Harmsen AG, Muggenburg BA, Snipes MB, Bice DE (1985) The role of macrophages in particle translocation from lungs to lymph nodes. Science 230: 1277-1280.
44. Petti CA, Fowler VG Jr (2003) Staphylococcus aureus bacteremia and endocarditis. Cardiol Clin 21: 219-233.
45. Baughn R, Bonventre PF (1975) Phagocytosis and intracellular killing of Staphylococcus aureus by normal mouse peritoneal macrophages. Infect Immum 12: 346-352.
46. Hebert A, Sayasith K, Senechal S, Dubreuil P, Lagace J (2000) Demonstration of intracellular Staphylococcus aureus in bovine mastitis alveolar cells and macrophages isolated from naturally infected cow milk. FEMS Microbiol Lett 193: 57-62.
47. Jakab GJ, Green GM (1976) Defect in intracellular killing of Staphylococcus aureus within alveolar macrophages in Sendai virus-infected murine lungs. J Clin Invest 57: 1533-1539.
48. Michailova L, Stoitsova S, Markova N, Kussovski V, Jordanova M, et al.(2000) Interaction of alveolar macrophages with Staphylococcus aureus and induction of microbial L-forms during infection in rats. Int J Med Microbiol 290: 259-267.
49. Elliott GR, Peterson PK, Verbrugh HA, Freiberg MR, Hoidal JR, et al. (1982) Influence of subinhibitory concentrations of penicillin, cephalothin, and clindamycin on Staphylococcus aureus growth in human phagocytic cells. Antimicrob Agents Chemother 22: 781-784.
50. Ali F, Lee ME, Iannelli F, Pozzi G, Mitchell TJ, et al. (2003) Streplococcus pneumoniae-associated human macrophage apoptosis after bacterial internalization via complement and Fc-gamma receptors correlates with intracellular bacterial load. J Infect Dis 188: 1119-1131.
51. Koterski JF, Nahvi M, Venkatesan MM, Haimovich B (2005) Virulent Shigella flexneri causes damage to mitochondria and triggers necrosis in infected human monocyte-derived macrophages. Infect Immun 73: 504-513.
52. Monack DM, Raupach B, Hromocky AE, Falkow S (1996) Salmonella typhimurium invasion induces apoptesis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
53. Monack DM, Mecsas J, Ghori N, Falkow S (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci USA 94: 10385-10390.
54. Sun GW, Lu J, Pervaiz S, Cao WP, Gan YH (2005) Caspase-1 dependent macrophage death induced by Burkholderia pseudomallei Cell Microbiol 7: 1447-1458.
55. Zychlinsky A, Prevost MC, Sansonetti PJ (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.
56. Sabat A, Krzysztoń-Russjan J, Strzałka W, Filipek R, Koscwska K, et al. (2003) New method for typing Staphylococcus aureus strains: multiple-locus variable-number tandem repeat analysis of polymorphism and genetic relationships of clinical isolates. J Clin Microbiol 41: 1801-1804.
57. Decker T, Muller M, Stockinger S (2005) The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 5: 675-687.
58. Gruenberg J, van der Goot FG (2006) Mechanisms of pathogen entry through the endosomal compartments. Nat Rev Mol Cell Biol 7: 495-504.
59. Rosenberger CM, Finley B (2003) Phagocyte sabotage:disruption of macrophage signalling by bacterial pathogens. Nat Rev Mol Cell Biol 4: 385-396.
60. Giachino P, Engelmann S, Bischoff M (2001) Sigma(B) activity depends on RsbU Staphylococcus aureus. J Bacteriol 183: 1843-1852.
61. Horsburgh MJ, Aiah JL, White IJ, Shaw L, Lithgow JK, et al. (206) sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184: 5457-5467.
62. Shompole S, Henton KT, Liou LE, Dziewanowska K, Bohach GA, et al. (2003) Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing. Mol Microbiol 49: 919-927.
63. Alexander EH, Rivera FA, Marriott I, Anguita J, Bost KL (2003) Staphylococcus aureus-induced tumor necrosis factor-related apoptosis-inducing ligand expression mediates apoptosis and caspase-8 activation in infected osteoblasts. BMC Microbiol 2: 3-5.
64. Haslinger-Loffler B, Wagner B, Bruck M, Strangfeld K, Grundmeier M, et al. (2006) Staphylococcus aureus induces caspase-independent cell death in human peritoneal mesothelial cells. Kidney Int 70: 1089-1098.
65. Mempel M, Schopp C, Hojka M, Fesq H, Weidinger S, et al. (2002) Invasion of human keratinocytes by Staphylococcus aureus and intracellular bacterial persistence represent haemolysin-independent virulence mechanism that are followed by features of necrotic and apoptotic keratinocyte cell death. Br J Dermatol 146: 943-51.
66. Baran J, Weglarczyk K, Mysiak M, Guzik K, Ernst M, et al.(2001) Fas (CD95)-Fas ligand interactions are responsible for monocyte apoptosis occurring as a result of phagocytosis and killing of Staphylococcus aureus. Infect Immun 69: 1287-1297.
67. Weglarczyk K, Baran J, Zembala M, Pryjma J (2004) Caspase-8 activation precedes alterations of mitochondrial membrane potential during monocyte apoptosis induced by phagocytosis and killing of Staphylococcus aureus. Infect Immun 72: 2590-2597.
68. Stuart LM, Ezekowitz RA (2005) Phagocytosis: elegant complexity. Immunity 22: 539-550.
69. Underhill DM, Ozinsky A (2002) Phagocytosis of microbes: complexity in action. Annu Rev Immunol 20: 825-852.
70. Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, et al. (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170: 477-485.
71. Bischoff M, Dunman P, Kormanec J, Macapagal D, Murphy E, et al. (2004) Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J Bacteriol 186: 4085-4099.
72. Shaw LN, Aish J, Davenport JE, Brown MC, Lithgow JK, et al. (2006) Investigations into sigmaB-modulated regulatory pathways governing extracellular virulence determinant production in Staphylococcus aureus. J Bacteriol 188: 6070-6080.
73. Liu GY, Essex A, Buchanan JT, Datta V, Hoffman HM, et al. (2005) Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med 202: 209-215.
74. Qazi SN, Counil E, Morrissey J, Rees CE, Cockayne A, et al. (2001) agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect Immun 69: 7074-7082.
75. Dunman PM, Murphy E, Haney S, Palacios D, Tuckcr-Kellogg G, et al. (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr.and/or sarA loci. J Bacteriol 183: 7341-7353.
76. Bantel H, Sinha B, Domschke W, Peters G, Schulze-Osthoff K, et al. (2001) alpha-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J Cell Biol 155: 637-648.
77. Burlak C, Hammer CH, Robinson MA, Whitney AR, McGavin MJ, et al. (2007) Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced in vitro and during infection. Cell Microbiol 9: 1172-1190.
78. Menzies BE, Kourteva I (2000) Staphylococcus aureus alpha-toxin induces apoptosis in endothelial cells. FEMS Immunol Med Microbiol 29: 39-45.
79. Shaw L, Golonka E, Potempa J, Foster SJ (2004) The role and regulation of the extracellular proteases of Staphylococcus aureus Microbiology 150: 217 228.
80. Grundmeier M, Hussain M, Becker P, Heilmann C, Peters G, et al. (2004) Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect Immun 72: 7155-7163.
81. Gómez MI, Lee A, Reddy B, Muir A, Soong G, Pitt A, Cheung A, Prince A (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1 Nat Med. 10: 842-849.
82. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, et al. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
83. Drevets DA (1999) Dissemination of Listeria monogtogenes by infected phagocytes. Infect immun 67: 3512-3517.
84. Join-Lambert OF, Ezine S, Le Monnier A, Jaubert F, Okabe M, et al. (2005) Listeria monocytogenes-infected bone marrow myeloid cells promote bacterial invasion of the central nervous system. Cell Microbiol 7: 167-180.
85. Russell DG (2007) Who puts the tubercle in tuberculosis? Nat Rev Microbiol 5: 39-47.
86. Guzik K, Bzowska M, Smagur J, Krupa O, Sieprawska M, et al. (2007) A new insight into phagocytosis of apoptotic cells: proteolytic enzymes divert the recognition and clearance of polymorphonuclear leukocytes by macrophages. Cell Death Differ 14: 171-182.
87. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolacity for use in electron microscopy. J. Cell Biol 27: 137-138a.