Chitinases are negative regulators of Francisella novicida biofilms

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Chung, Myung Chul ^a   Dean, Scott ^a   Marakasova, Ekaterina S ^a   Nwabueze, Albert O ^a   Van Hoek, Monique L ^a  

^a GEORGE MASON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE; CONCANAVALIN A; DEOXYRIBONUCLEASE; EPITOPE; EXOPOLYSACCHARIDE; GENTAMICIN; PROTEINASE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; BIOPHYSICS; CELL INVASION; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME REGULATION; FRANCISELLA NOVICIDA; HUMAN; HUMAN CELL; HYDROPHOBICITY; LECTIN BINDING; NONHUMAN; PROTEIN BINDING; PROTEIN CLEAVAGE; SPECIES INVASION; CELL LINE; DRUG EFFECTS; FRANCISELLA; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CELL LINE; CHITINASE; FRANCISELLA; GENTAMICINS; HUMANS; MUTATION;

EID: 84899745510     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093119     Document Type: Article

References (44)

1. Bryers JD (2008) Medical biofilms. Biotechnol Bioeng 100: 1-18
2. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54: 49-79.
3. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95-108. (Pubitemid 39490064)
4. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
5. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322. (Pubitemid 29289651)
6. Liu J, Zogaj X, Barker JR, Klose KE (2007) Construction of targeted insertion mutations in Francisella tularensis subsp. novicida. BioTechniques43: 487 492.
7. Durham-Colleran MW, Verhoeven AB, van Hoek ML (2010) Francisella novicida forms in vitro biofilms mediated by an orphan response regulator. Microb Ecol 59: 457-465.
8. Margolis JJ, El-Etr S, Joubert LM, Moore E, Robison R, et al. (2010) Contributions of Francisella tularensis subsp. novicida chitinases and Sec secretion system to biofilm formation on chitin. Appl Environ Microbiol 76: 596-608.
9. Verhoeven AB, Durham-Colleran MW, Pierson T, Boswell WT, van Hoek ML (2010) Francisella philomiragia biofilm formation and interaction with the aquatic protist Acanthamoeba castellanii. Biol Bull 219: 178-188.
10. van Hoek ML (2013) Biofilms: An advancement in our understanding of Francisella species. Virulence 4: 833-846.
11. Mahajan UV, Gravgaard J, Turnbull M, Jacobs DB, McNealy TL (2011) Larval exposure to Francisella tularensis LVS affects fitness of the mosquito Culex quinquefasciatus. FEMS Microbiol Ecol 78: 520-530.
12. Arakane Y, Muthukrishnan S (2010) Insect chitinase and chitinase-like proteins. Cell Mol Life Sci 67: 201-216.
13. Kasprzewska A (2003) Plant chitinases - regulation and function. Cell Mol Biol Lett 8: 809-824.
14. Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, et al. (2011) Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol 73: 479-501.
15. Dahiya N, Tewari R, Hoondal GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol 71: 773-782. (Pubitemid 44162510)
16. Chandler JC, Molins CR, Petersen JM, Belisle JT (2011) Differential chitinase activity and production within Francisella species, subspecies, and subpopulations. J Bacteriol 193: 3265-3275.
17. Palmer JS, Flint SH, Schmid J, Brooks JD (2010) The role of surface charge and hydrophobicity in the attachment of Anoxybacillus flavithermus isolated from milk powder. J Ind Microbiol Biotechnol 37: 1111-1119.
18. Bellon-Fontaine MN, Raulta J, van Oss CJ (1996) Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids Surf B Biointerfaces 7: 47-53.
19. Vogel R, Willmott G, Kozak D, Roberts GS, Anderson W, et al. (2011) Quantitative sizing of nano/microparticles with a tunable elastomeric pore sensor. Anal Chem 83: 3499-506.
20. Kozak D, Anderson W, Vogel R, Chen S, Antaw F, et al. (2012) Simultaneous size and ζ-potential measurements of individual nanoparticles in dispersion using size-tunable pore sensors. ACS Nano 6: 6990-7.
21. Sower SJ, Broom MF, Petersen GB (2007) Dynamically resizable nanometre-scale apertures for molecular sensing. Sens Actuators B Chem 123: 325-330. (Pubitemid 46497709)
22. Sutherland I (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147: 3-9.
23. Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, et al. (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279: 54881-54886. (Pubitemid 40053234)
24. Skillman LC, Sutherland IW, Jones MV (1998) The role of exopolysaccharides in dual species biofilm development. J Appl Microbiol 85: 13S-18S.
25. Orgad O, Oren Y, Walker SL, Herzberg M (2011) The role of alginate in Pseudomonas aeruginosa EPS adherence, viscoelastic properties and cell attachment. Biofouling 27: 787-798.
26. Johnsen AR, Hausner M, Schnell A, Wuertz S (2000) Evaluation of fluorescently labeled lectins for noninvasive localization of extracellular polymeric substances in Sphingomonas biofilms. Appl Environ Microbiol 66: 3487-3491. (Pubitemid 30627448)
27. Pantoom S, Vetter IR, Prinz H, Suginta W (2011) Potent family-18 chitinase inhibitors: x-ray structures, affinities, and binding mechanisms. J Biol Chem 286: 24312-24323.
28. Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47: 317-323. (Pubitemid 36070381)
29. Valle J, Latasa C, Gil C, Toledo-Arana A, Solano C, et al. (2012) Bap, a biofilm matrix protein of Staphylococcus aureus prevents cellular internalization through binding to GP96 host receptor. PLoS Pathog 8: e1002843.
30. Kraemer PS, Mitchell A, Pelletier MR, Gallagher LA, Wasnick M, et al. (2009) Genome-wide screen in Francisella novicida for genes required for pulmonary and systemic infection in mice. Infect Immun 77: 232-244.
31. Weiss DS, Brotcke A, Henry T, Margolis JJ, Chan K, et al. (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci USA 104: 6037-6042. (Pubitemid 47175654)
32. Hager AJ, Bolton DL, Pelletier MR, Brittnacher MJ, Gallagher LA, et al. (2006) Type IV pili-mediated secretion modulates Francisella virulence. Mol Microbiol 62: 227-237. (Pubitemid 44386562)
33. Bos R, van der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions - its mechanisms and methods for study. FEMS Microbiol Rev 23: 179-230.
34. Melillo A, Sledjeski DD, Lipski S, Wooten RM, Basrur V, et al. (2006) Identification of a Francisella tularensis LVS outer membrane protein that confers adherence to A549 human lung cells. FEMS Microbiol Lett 263: 102-108. (Pubitemid 44357708)
35. Hall JD, Craven RR, Fuller JR, Pickles RJ, Kawula TH (2007) Francisella tularensis replicates within alveolar type II epithelial cells in vitro and in vivo following inhalation. Infect Immun 75: 1034-1039. (Pubitemid 46203469)
36. Thethi K, Duszyk M (1997) Decreased cell surface charge in cystic fibrosis epithelia. Cell Biochem Funct 15: 35-38. (Pubitemid 27116530)
37. Keyhani NO, Roseman S (1999) Physiological aspects of chitin catabolism in marine bacteria. Biochim Biophys Acta 1473: 108-122.
38. Zogaj X, Wyatt GC, Klose KE (2012) Cyclic di-GMP stimulates biofilm formation and inhibits virulence of Francisella novicida. Infect Immun 80: 4239-4247.
39. Reif KE, Palmer GH, Ueti MW, Scoles GA, Margolis JJ, et al. (2011) Dermacentor andersoni transmission of Francisella tularensis subsp. novicida reflects bacterial colonization, dissemination, and replication coordinated with tick feeding. Infect Immun 79: 4941-4946.
40. Heydorn A, Ersbøll BK, Hentzer M, Parsek MR, Givskov M, et al. (2000) Experimental reproducibility in flow-chamber biofilms. Microbiology 146: 2409-2415.
41. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, et al. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407.
42. Rahman MM, Kim WS, Kumura H, Shimazaki K (2008) Autoaggregation and surface hydrophobicity of bifidobacteria. World J Microbiol Biotechnol 24: 1593-1598.
43. Vogel R, Anderson W, Eldridge J, Glossop B, Willmott G (2012) A variable pressure method for characterizing nanoparticle surface charge using pore sensors. Anal Chem 84: 3125-3131.
44. Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S, et al. (2005) Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal Biochem 339: 69-72. (Pubitemid 40342680)