Biofilm formed by a hypervirulent (hypermucoviscous) variant of Klebsiella pneumoniae does not enhance serum resistance or survival in an in vivo abscess model

Virulence

Volumn 3, Issue 3, 2012, Pages 309-318

  Kong, Qingli ^a,b   Beanan, Janet M ^a   Olson, Ruth ^a   Mac, UlrikeDonald ^a   Shon, Alyssa S ^a   Metzger, Daniel J ^a   Pomakov, Alexander O ^a   Russo, Thomas A ^a,c  

^a UNIVERSITY AT BUFFALO   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c VA WESTERN NEW YORK HEALTHCARE SYSTEM   (United States)

Author keywords

Abscess model; Animal model; Biofilm; Complement; Hypermucoviscous; Hypervirulent; Klebsiella pneumoniae; Virulence

Indexed keywords

GLUTAMATE AMMONIA LIGASE; GLYCEROL; SUCCINYL COENZYME A SYNTHETASE; SUCCINYL COENZYME A SYNTHETASE ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASCITES; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BIOFILM; CONTROLLED STUDY; IN VIVO STUDY; KLEBSIELLA PNEUMONIAE; NONHUMAN; OPERON; QUANTITATIVE ANALYSIS; RAT; SERUM; SKIN ABSCESS; SURVIVAL;

ANIMALIA; KLEBSIELLA PNEUMONIAE; RATTUS;

EID: 84862855657     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Fung CP, Chang FY, Lee SC, Hu BS, Kuo BI, Liu CY, et al. A global emerging disease of Klebsiella pneumoniae liver abscess: is serotype K1 an important factor for complicated endophthalmitis?. Gut 2002; 50:420-4; PMID: 11839725; DOI: 10.1136/gut.50.3.420.
2. Keynan Y, Karlowsky JA, Walus T, Rubinstein E. Pyogenic liver abscess caused by hypermucoviscous Klebsiella pneumoniae. Scand J Infect Dis 2007; 39:828-30; PMID: 17701725; DOI: 10.1080/00365540701266763.
3. Lederman ER, Crum NF. Pyogenic liver abscess with a focus on Klebsiella pneumoniae as a primary pathogen: an emerging disease with unique clinical characteristics. Am J Gastroenterol 2005; 100:322-31; PMID: 15667489; DOI: 10.1111/j.1572-0241.2005.40310.x.
4. Turton JF, Englender H, Gabriel SN, Turton SE, Kaufmann ME, Pitt TL. Genetically similar isolates of Klebsiella pneumoniae serotype K1 causing liver abscesses in three continents. J Med Microbiol 2007; 56:593-7; PMID: 17446279; DOI: 10.1099/jmm.0.46964-0.
5. Pomakova DK, Hsiao CB, Beanan JM, Olson R, Macdonald U, Keynan Y, et al. Clinical and phenotypic differences between classic and hypervirulent Klebsiella pneumonia: an emerging and under-recognized pathogenic variant. Eur J Clin Microbiol Infect Dis 2011;; PMID: 21918907; DOI: 10.1007/s10096-011-1396-6.
6. Decré D, Verdet C, Emirian A, Le Gourrierec T, Petit JC, Offenstadt G, et al. Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. J Clin Microbiol 2011; 49:3012-4; PMID: 21677064; DOI: 10.1128/JCM.00676-11.
7. Fang CT, Lai SY, Yi WC, Hsueh PR, Liu KL, Chang SC. Klebsiella pneumoniae genotype K1: an emerging pathogen that causes septic ocular or central nervous system complications from pyogenic liver abscess. Clin Infect Dis 2007; 45:284-93; PMID: 17599305; DOI: 10.1086/519262.
8. Liu YC, Cheng DL, Lin CL. Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med 1986; 146:1913-6; PMID: 3532983; DOI: 10.1001/archinte.1986.00360220057011.
9. Wang JH, Liu YC, Lee SS, Yen MY, Chen YS, Wang JH, et al. Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis 1998; 26:1434-8; PMID: 9636876; DOI: 10.1086/516369.
10. Han SH. Review of hepatic abscess from Klebsiella pneumoniae. An association with diabetes mellitus and septic endophthalmitis. West J Med 1995; 162:220-4; PMID: 7725704.
11. Chang FY, Chou MY. Comparison of pyogenic liver abscesses caused by Klebsiella pneumoniae and non-K. pneumoniae pathogens. J Formos Med Assoc 1995; 94:232-7; PMID: 7613255.
12. Cheng DL, Liu YC, Yen MY, Liu CY, Wang RS. Septic metastatic lesions of pyogenic liver abscess. Their association with Klebsiella pneumoniae bacteremia in diabetic patients. Arch Intern Med 1991; 151:1557-9; PMID: 1872659; DOI: 10.1001/archinte.1991.00400080059010.
13. Dylewski JS, Dylewski I. Necrotizing fasciitis with Klebsiella liver abscess. Clin Infect Dis 1998; 27:1561-2; PMID: 9868697; DOI: 10.1086/517760.
14. Chen CH, Huang WC, Chen TY, Hung TT, Liu HC, Chen CH. Massive necrotizing pneumonia with pulmonary gangrene. Ann Thorac Surg 2009; 87:310-1; PMID: 19101324; DOI: 10.1016/j.athoracsur.2008.05.077.
15. Ku YH, Chuang YC, Yu WL. Clinical spectrum and molecular characteristics of Klebsiella pneumoniae causing community-acquired extrahepatic abscess. J Microbiol Immunol Infect 2008; 41:311-7; PMID: 18787738.
16. Ko WC, Paterson DL, Sagnimeni AJ, Hansen DS, Von Gottberg A, Mohapatra S, et al. Community-acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerg Infect Dis 2002; 8:160-6; PMID: 11897067; DOI: 10.3201/eid0802.010025.
17. Fang CT, Chen YC, Chang SC, Sau WY, Luh KT. Klebsiella pneumoniae meningitis: timing of antimicrobial therapy and prognosis. QJM 2000; 93:45-53; PMID: 10623782; DOI: 10.1093/qjmed/93.1.45.
18. Yeh KM, Kurup A, Siu LK, Koh YL, Fung CP, Lin JC, et al. Capsular serotype K1 or K2, rather than magA and rmpA, is a major virulence determinant for Klebsiella pneumoniae liver abscess in Singapore and Taiwan. J Clin Microbiol 2007; 45:466-71; PMID: 17151209; DOI: 10.1128/JCM.01150-06.
19. Brisse S, Fevre C, Passet V, Issenhuth-Jeanjean S, Tournebize R, Diancourt L, et al. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization. PLoS One 2009; 4:e4982; PMID: 19319196; DOI: 10.1371/journal.pone.0004982.
20. Wu KM, Li LH, Yan JJ, Tsao N, Liao TL, Tsai HC, et al. Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J Bacteriol 2009; 191:4492-501; PMID: 19447910; DOI: 10.1128/JB.00315-09.
21. Nassif X, Sansonetti PJ. Correlation of the virulence of Klebsiella pneumoniae K1 and K2 with the presence of a plasmid encoding aerobactin. Infect Immun 1986; 54:603-8; PMID: 2946641.
22. Hsu CR, Lin TL, Chen YC, Chou HC, Wang JT. The role of Klebsiella pneumoniae rmpA in capsular polysaccharide synthesis and virulence revisited. Microbiology 2011; 157:3446-57; PMID: 21964731; DOI: 10.1099/mic.0.050336-0.
23. Hsieh PF, Lin TL, Lee CZ, Tsai SF, Wang JT. Serum-induced iron-acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 2008; 197:1717-27; PMID: 18433330; DOI: 10.1086/588383.
24. Russo TA, Shon AS, Beanan JM, Olson R, MacDonald U, Pomakov AO, et al. Hypervirulent K. pneumoniae secretes more and more active iron-acquisition molecules than "classical" K. pneumoniae thereby enhancing its virulence. PLoS One 2011; 6:e26734; PMID: 22039542; DOI: 10.1371/journal.pone.0026734.
25. King LB, Swiatlo E, Swiatlo A, McDaniel LS. Serum resistance and biofilm formation in clinical isolates of Acinetobacter baumannii. FEMS Immunol Med Microbiol 2009; 55:414-21; PMID: 19220466; DOI: 10.1111/j.1574-695X.2009.00538.x.
26. Simmons WL, Dybvig K. Biofilms protect Mycoplasma pulmonis cells from lytic effects of complement and gramicidin. Infect Immun 2007; 75:3696-9; PMID: 17517864; DOI: 10.1128/IAI.00440-07.
27. Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol 2005; 13:34-40; PMID: 15639630; DOI: 10.1016/j.tim.2004.11.010.
28. Wu MC, Lin TL, Hsieh PF, Yang HC, Wang JT. Isolation of genes involved in biofilm formation of a Klebsiella pneumoniae strain causing pyogenic liver abscess. PLoS One 2011; 6:e23500; PMID: 21858144; DOI: 10.1371/journal.pone.0023500.
29. Bakaletz LO. Bacterial biofilms in otitis media: evidence and relevance. Pediatr Infect Dis J 2007; 26:S17-9; PMID: 18049376; DOI: 10.1097/INF.0b013e318154b273.
30. Ricucci D, Siqueira JF. Biofilms and apical periodontitis: study of prevalence and association with clinical and histopathologic findings. J Endod 2010; 36:1277-88; PMID: 20647081; DOI: 10.1016/j.joen.2010.04.007.
31. Yamanaka T, Yamane K, Furukawa T, Matsumoto-Mashimo C, Sugimori C, Nambu T, et al. Comparison of the virulence of exopolysaccharide-producing Prevotella intermedia to exopolysaccharide non-producing periodontopathic organisms. BMC Infect Dis 2011; 11:228; PMID: 21864411; DOI: 10.1186/1471-2334-11-228.
32. Pan PC, Chen HW, Wu PK, Wu YY, Lin CH, Wu JH. Mutation in fucose synthesis gene of Klebsiella pneumoniae affects capsule composition and virulence in mice. Exp Biol Med (Maywood) 2011; 236:219-26; PMID: 21321319; DOI: 10.1258/ebm.2010.010193.
33. Langstraat J, Bohse M, Clegg S. Type 3 fimbrial shaft (MrkA) of Klebsiella pneumoniae, but not the fimbrial adhesin (MrkD), facilitates biofilm formation. Infect Immun 2001; 69:5805-12; PMID: 11500458; DOI: 10.1128/IAI.69.9.5805-5812.2001.
34. Wilksch JJ, Yang J, Clements A, Gabbe JL, Short KR, Cao H, et al. MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog 2011; 7:e1002204; PMID: 21901098; DOI: 10.1371/journal.ppat.1002204.
35. Boddicker JD, Anderson RA, Jagnow J, Clegg S. Signature-tagged mutagenesis of Klebsiella pneumoniae to identify genes that influence biofilm formation on extracellular matrix material. Infect Immun 2006; 74:4590-7; PMID: 16861646; DOI: 10.1128/IAI.00129-06.
36. Balestrino D, Ghigo JM, Charbonnel N, Haagensen JA, Forestier C. The characterization of functions involved in the establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides. Environ Microbiol 2008; 10:685-701; PMID: 18237304; DOI: 10.1111/j.1462-2920.2007.01491.x.
37. Stahlhut SG, Schroll C, Harmsen M, Struve C, Krogfelt KA. Screening for genes involved in Klebsiella pneumoniae biofilm formation using a fosmid library. FEMS Immunol Med Microbiol 2010; 59:521-4; PMID: 20482632.
38. Hennequin C, Forestier C. oxyR, a LysR-type regulator involved in Klebsiella pneumoniae mucosal and abiotic colonization. Infect Immun 2009; 77:5449-57; PMID: 19786563; DOI: 10.1128/IAI.00837-09.
39. Yamazaki Y, Danelishvili L, Wu M, Macnab M, Bermudez LE. Mycobacterium avium genes associated with the ability to form a biofilm. Appl Environ Microbiol 2006; 72:819-25; PMID: 16391123; DOI: 10.1128/AEM.72.1.819-825.2006.
40. Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 2004; 51:659-74; PMID: 14731270; DOI: 10.1046/j.1365-2958.2003.03865.x.
41. Mukherjee J, Ow SY, Noirel J, Biggs CA. Quantitative protein expression and cell surface characteristics of Escherichia coli MG1655 biofilms. Proteomics 2011; 11:339-51; PMID: 21268264; DOI: 10.1002/pmic.201000386.
42. Wagstaff JL, Sadovskaya I, Vinogradov E, Jabbouri S, Howard MJ. Poly-N-acetylglucosamine and poly(glycerol phosphate) teichoic acid identification from staphylococcal biofilm extracts using excitation sculptured TOCSY NMR. Mol Biosyst 2008; 4:170-4; PMID: 18213410; DOI: 10.1039/b715242f.
43. Sadovskaya I, Vinogradov E, Li J, Jabbouri S. Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr Res 2004; 339:1467-73; PMID: 15178389; DOI: 10.1016/j.carres.2004.03.017.
44. Vogt M, Flemming HC, Veeman WS. Diffusion in Pseudomonas aeruginosa biofilms: a pulsed field gradient NMR study. J Biotechnol 2000; 77:137-46; PMID: 10674220; DOI: 10.1016/S0168-1656(99)00213-8.
45. Coulon C, Vinogradov E, Filloux A, Sadovskaya I. Chemical analysis of cellular and extracellular carbohydrates of a biofilm-forming strain Pseudomonas aeruginosa PA14. PLoS One 2010; 5:e14220; PMID: 21151973; DOI: 10.1371/journal.pone.0014220.
46. Sadovskaya I, Vinogradov E, Li J, Hachani A, Kowalska K, Filloux A. High-level antibiotic resistance in Pseudomonas aeruginosa biofilm: the ndvB gene is involved in the production of highly glycerol-phosphorylated beta-(1->3)-glucans, which bind aminoglycosides. Glycobiology 2010; 20:895-904; PMID: 20348539; DOI: 10.1093/glycob/cwq047.
47. Russo TA, MacDonald U, Beanan JM, Olson R, MacDonald IJ, Sauberan SL, et al. Penicillin-binding protein 7/8 contributes to the survival of Acinetobacter baumannii in vitro and in vivo. J Infect Dis 2009; 199:513-21; PMID: 19143563; DOI: 10.1086/596317.
48. Russo TA, Carlino UB, Mong A, Jodush ST. Identification of genes in an extraintestinal isolate of Escherichia coli with increased expression after exposure to human urine. Infect Immun 1999; 67:5306-14; PMID: 10496910.
49. Russo TA, Beanan JM, Olson R, MacDonald U, Luke NR, Gill SR, et al. Rat pneumonia and soft-tissue infection models for the study of Acinetobacter baumannii biology. Infect Immun 2008; 76:3577-86; PMID: 18541654; DOI: 10.1128/IAI.00269-08.
50. Dalhoff A, Frank G, Luckhaus G. The granuloma pouch: an in vivo model for pharmacokinetic and chemotherapeutic investigations. I. Biochemical and histological characterization. Infection 1982; 10:354-60; PMID: 7152686; DOI: 10.1007/BF01642299.
51. Dalhoff A, Frank G, Luckhaus G. The granuloma pouch: an in vivo model for pharmacokinetic and chemotherapeutic investigations. II. Microbiological characterization. Infection 1983; 11:41-6; PMID: 6188702; DOI: 10.1007/BF01651357.
52. Russo TA, Liang Y, Cross AS. The presence of K54 capsular polysaccharide increases the pathogenicity of Escherichia coli in vivo. J Infect Dis 1994; 169:112-8; PMID: 8277173; DOI: 10.1093/infdis/169.1.112.