Cigarette smoke increases Staphylococcus aureus biofilm formation via oxidative stress

Infection and Immunity

Volumn 80, Issue 11, 2012, Pages 3804-3811

  Kulkarni, Ritwij ^a   Antala, Swati ^a   Wang, Alice ^a   Amaral, Fábio E ^a   Rampersaud, Ryan ^a   LaRussa, Samuel J ^a   Planet, Paul J ^a   Ratner, Adam J ^a  

^a Howard Hughes Medical Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIGARETTE SMOKE; DEOXYRIBONUCLEASE; FIBRONECTIN BINDING PROTEIN; FREE RADICAL; HYDROGEN PEROXIDE; OXIDOREDUCTASE; PROTEINASE K; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; CELL ADHESION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN STABILITY; QUORUM SENSING; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION INITIATION;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; BIOFILMS; CELL LINE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; OXIDATIVE STRESS; SMOKING; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 84867605281     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00689-12     Document Type: Article

References (76)

1. Antunes MB, et al. 2012. Molecular basis of tobacco-induced bacterial biofilms. Otolaryngol. Head Neck Surg. doi:10.1177/0194599812447263.
2. Bagaitkar J, et al. 2011. Tobacco smoke augments Porphyromonas gingivalis-Streptococcus gordonii biofilm formation. PLoS One 6:e27386. doi: 10.1371/journal.pone.0027386.
3. Bagaitkar J, et al. 2009. Tobacco-induced alterations to Porphyromonas gingivalis-host interactions. Environ. Microbiol. 11:1242-1253.
4. Baker J, et al. 2010. Copper stress induces a global stress response in Staphylococcus aureus and represses sae and agr expression and biofilm formation. Appl. Environ. Microbiol. 76:150-160.
5. Beenken KE, Blevins JS, Smeltzer MS. 2003. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71:4206-4211.
6. Birrell MA, Wong S, Catley MC, Belvisi MG. 2008. Impact of tobaccosmoke on key signaling pathways in the innate immune response in lung macrophages. J. Cell. Physiol. 214:27-37.
7. Blevins JS, et al. 2003. Role of sarA in the pathogenesis of Staphylococcus aureus musculoskeletal infection. Infect. Immun. 71:516-523.
8. Bogaert D, et al. 2004. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 363:1871-1872.
9. Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4:e1000052. doi:10.1371/journal.ppat.1000052.
10. Boucher H, Miller LG, Razonable RR. 2010. Serious infections caused by methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 51(Suppl. 2): S183-S197.
11. Centers for Disease Control and Prevention. 2011. Current cigarette smoking prevalence among working adults-United States, 2004-2010. MMWR. Morb. Mortal. Wkly. Rep. 60:1305-1309.
12. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ. 2004. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol. Medical Microbiol. 40:1-9.
13. Cheung AL, Chien YT, Bayer AS. 1999. Hyperproduction of alphahemolysin in a sigB mutant is associated with elevated SarA expression in Staphylococcus aureus. Infect. Immun. 67:1331-1337.
14. 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.
15. Church DF, Pryor WA. 1985. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ. Health Perspect. 64:111-126.
16. Cosgrove K, et al. 2007. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J. Bacteriol. 189:1025-1035.
17. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
18. Croes S, et al. 2009. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol. 9:229. doi:10.1186/1471-2180-9-229.
19. Cucarella C, et al. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-2896.
20. Cue D, et al. 2009. Rbf promotes biofilm formation by Staphylococcus aureus via repression of icaR, a negative regulator of icaADBC. J. Bacteriol. 191:6363-6373.
21. Davey ME, O'Toole AG. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847-867.
22. Downs CA, Montgomery DW, Merkle CJ. 2011. Age-related differences in cigarette smoke extract-induced H2O2 production by lung endothelial cells. Microvasc. Res. 82:311-317.
23. Dziewanowska K, 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.
24. Ebbert JO, Croghan IT, Schroeder DR, Murawski J, Hurt RD. 2007. Association between respiratory tract diseases and secondhand smoke exposure among never smoking flight attendants: a cross-sectional survey. Environ. Health 6:28.
25. Feng Y, et al. 2011. Exposure to cigarette smoke inhibits the pulmonary T-cell response to influenza virus and Mycobacterium tuberculosis. Infect. Immun. 79:229-237.
26. Frees D, et al. 2004. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol. Microbiol. 54:1445-1462.
27. Goldstein-Daruech N, et al. 2011. Tobacco smoke mediated induction of sinonasal microbial biofilms. PLoS One 6:e15700. doi:10.1371/ journal.pone.0015700.
28. Gross M, Cramton SE, Gotz F, Peschel A. 2001. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 69:3423-3426.
29. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. 2006. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368:874-885.
30. Grundmeier M, 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.
31. Haggar A, et al. 2003. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect. Immun. 71:2310-2317.
32. Heilmann C. 2011. Adhesion mechanisms of staphylococci. Adv. Exp. Med. Biol. 715:105-123.
33. Huvenne W, et al. 2011. Exacerbation of cigarette smoke-induced pulmonary inflammation by Staphylococcus aureus enterotoxin B in mice. Respir. Res. 12:69.
34. Jefferson KK, Pier DB, Goldmann DA, Pier GB. 2004. The teicoplaninassociated locus regulator (TcaR) and the intercellular adhesin locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus. J. Bacteriol. 186:2449-2456.
35. Jorgensen E, et al. 2008. Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 8:229. doi:10.1186/1471-2407-8-229.
36. Karavolos MH, Horsburgh MJ, Ingham E, Foster SJ. 2003. Role and regulation of the superoxide dismutases of Staphylococcus aureus. Microbiology 149:2749-2758.
37. Kulkarni R, et al. 2010. Cigarette smoke inhibits airway epithelial cell innate immune responses to bacteria. Infect. Immun. 78:2146-2152.
38. Kumar PS, Matthews CR, Joshi V, de Jager M, Aspiras M. 2011. Tobacco smoking affects bacterial acquisition and colonization in oral biofilms. Infect. Immun. 79:4730-4738.
39. Lim Y, Jana M, Luong TT, Lee CY. 2004. Control of glucoseand NaCl-induced biofilm formation by rbf in Staphylococcus aureus. J. Bacteriol. 186:722-729.
40. Littman DR, Pamer EG. 2011. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 10: 311-323.
41. Lowy FD. 2003. Antimicrobial resistance: the example of Staphylococcus aureus. J. Clin. Invest. 111:1265-1273.
42. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
43. Luong TT, Lei MG, Lee CY. 2009. Staphylococcus aureus Rbf activates biofilm formation in vitro and promotes virulence in a murine foreign body infection model. Infect. Immun. 77:335-340.
44. Macnee W, Rahman I. 1999. Oxidants and antioxidants as therapeutic targets in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 160:S58-65.
45. McMaster SK, et al. 2008. Cigarette smoke inhibits macrophage sensing of Gram-negative bacteria and lipopolysaccharide: relative roles of nicotine and oxidant stress. Br. J. Pharmacol. 153:536-543.
46. Melles DC, et al. 2007. Nasopharyngeal co-colonization with Staphylococcus aureus and Streptococcus pneumoniae in children is bacterial genotype independent. Microbiology 153:686-692.
47. Menzies BE. 2003. The role of fibronectin binding proteins in the pathogenesis of Staphylococcus aureus infections. Curr. Opin. Infect. Dis. 16: 225-229.
48. Mercer BA, Kolesnikova N, Sonett J, D'Armiento J. 2004. Extracellular regulated kinase/mitogen activated protein kinase is up-regulated in pulmonary emphysema and mediates matrix metalloproteinase-1 induction by cigarette smoke. J. Biol. Chem. 279:17690-17696.
49. Miller KD, Hetrick DL, Bielefeldt DJ. 1977. Production and properties of Staphylococcus aureus (strain Newman D2C) with uniform clumping factor activity. Thromb. Res. 10:203-211.
50. Murphy TF, Bakaletz LO, Smeesters PR. 2009. Microbial interactions in the respiratory tract. Pediatr. Infect. Dis. J. 28:S121-126.
51. Mutepe ND, et al. 2012. Effects of cigarette smoke condensate on pneumococcal biofilm formation and pneumolysin. Eur. Respir. J. doi:10.1183/ 09031936.00213211.
52. Novick RP, Geisinger E. 2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42:541-564.
53. Olsen K, et al. 2012. Staphylococcus aureus nasal carriage is associated with serum 25-hydroxyvitamin D levels, gender and smoking status. The Tromso Staph and Skin Study. Eur. J. Clin. Microbiol. Infect. Dis. 31:465-473.
54. Peng HL, Novick RP, Kreiswirth B, Kornblum J, Schlievert P. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170:4365-4372.
55. Periasamy S, et al. 2012. How Staphylococcus aureus biofilms develop their characteristic structure. Proc. Natl. Acad. Sci. U. S. A. 109:1281-1286.
56. Prasad DS, Kabir Z, Dash AK, Das BC. 2009. Smoking and cardiovascular health: a review of the epidemiology, pathogenesis, prevention and control of tobacco. Indian J. Med. Sci. 63:520-533.
57. Pryor WA, Stone K, Zang LY, Bermudez E. 1998. Fractionation of aqueous cigarette tar extracts: fractions that contain the tar radical cause DNA damage. Chem. Res. Toxicol. 11:441-448.
58. Rice KC, et al. 2007. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 104:8113-8118.
59. Shopsin B, et al. 2000. Prevalence of methicillin-resistant and methicillinsusceptible Staphylococcus aureus in the community. J. Infect. Dis. 182: 359-362.
60. Sinha B, et al. 1999. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin α5β1. Cell. Microbiol. 1:101-117.
61. Sopori M. 2002. Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2:372-377.
62. Stampfli MR, Anderson GP. 2009. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol. 9:377-384.
63. Sun F, et al. 2012. Quorum-sensing agr mediates bacterial oxidation response via an intramolecular disulfide redox switch in the response regulator AgrA. Proc. Natl. Acad. Sci. U. S. A. 109:9095-9100.
64. Tagawa Y, et al. 2008. Induction of apoptosis by cigarette smoke via ROS-dependent endoplasmic reticulum stress and CCAAT/enhancerbinding protein-homologous protein (CHOP). Free Radic. Biol. Med. 45: 50-59.
65. Tenover FC, Goering RV. 2009. Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J. Antimicrob. Chemother. 64:441-446.
66. Tote K, Horemans T, Vanden Berghe D, Maes L, Cos P. 2010. Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 76: 3135-3142.
67. Vassallo R, Kroening PR, Parambil J, Kita H. 2008. Nicotine and oxidative cigarette smoke constituents induce immune-modulatory and proinflammatory dendritic cell responses. Mol. Immunol. 45:3321-3329.
68. Vergara-Irigaray M, et al. 2009. Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect. Immun. 77:3978-3991.
69. Vuong C, Saenz HL, Gotz F, Otto M. 2000. Impact of the agr quorumsensing system on adherence to polystyrene in Staphylococcus aureus.J. Infect. Dis. 182:1688-1693.
70. Wang JT, et al. 2010. Incidence of and risk factors for communityassociated methicillin-resistant Staphylococcus aureus acquired infection or colonization in intensive-care-unit patients. J. Clin. Microbiol. 48: 4439-4444.
71. Warren CW, et al. 2008. Global youth tobacco surveillance, 2000-2007. MMWR Surveill. Summ. 57:1-28.
72. Wertheim HF, et al. 2005. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 5:751-762.
73. Yageta Y, et al. 2011. Role of Nrf2 in host defense against influenza virus in cigarette smoke-exposed mice. J. Virol. 85:4679-4690.
74. Yao H, Rahman I. 2011. Current concepts on oxidative/carbonyl stress, inflammation and epigenetics in pathogenesis of chronic obstructive pulmonary disease. Toxicol. Appl. Pharmacol. 254:72-85.
75. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP. 2004. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol. 186:1838-1850.
76. Zmantar T, Kouidhi B, Miladi H, Mahdouani K, Bakhrouf A. 2010. A microtiter plate assay for Staphylococcus aureus biofilm quantification at various pH levels and hydrogen peroxide supplementation. New Microbiol. 33:137-145.