Surface-Associated Lipoproteins Link Virulence to Colitogenic Activity in IL-10-Deficient Mice Independent of Their Expression Levels
Enterococcus faecalis is a commensal of the human intestinal core microbiota harboring several putative virulence factors, which highlight its role as opportunistic pathogen. This dualistic character is supported by recent evidence linking Enterococcus spp. to the pathogenesis of inflammatory bowel diseases (IBD). Although several studies suggest a crucial role for opportunistic pathogens in IBD pathogenesis targeting genetically susceptible individuals, the dynamic relationship between disease-relevant host compartments and specific bacterial structures able to trigger intestinal inflammation remain unclear. Here, we report that cell surface-associated lipoproteins and the enterococcal polysaccharide antigen, which are relevant for E. faecalis virulence in invertebrate infection models, but whose expression is minimally affected by the intestinal inflammatory milieu, exhibit colitogenic activity in a mouse model susceptible for chronic colitis. Bacterial lipoproteins trigger innate immune cell activation and are a critical prerequisite for E. faecalis-induced colitis. The enterococcal polysaccharide antigen mediates bacterial mucus penetration and adhesion to mucosal surfaces, promotes the formation of biofilm and contributes to E. faecalis colitogenic activity. Using E. faecalis as a model organism, we demonstrate that colitogenic activity of opportunistic pathogens can be assigned to specific bacterial structures, a finding that may help to identify the most essential steps in IBD-related microbe-host interactions.
Vyšlo v časopise:
Surface-Associated Lipoproteins Link Virulence to Colitogenic Activity in IL-10-Deficient Mice Independent of Their Expression Levels. PLoS Pathog 11(6): e32767. doi:10.1371/journal.ppat.1004911
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004911
Souhrn
Enterococcus faecalis is a commensal of the human intestinal core microbiota harboring several putative virulence factors, which highlight its role as opportunistic pathogen. This dualistic character is supported by recent evidence linking Enterococcus spp. to the pathogenesis of inflammatory bowel diseases (IBD). Although several studies suggest a crucial role for opportunistic pathogens in IBD pathogenesis targeting genetically susceptible individuals, the dynamic relationship between disease-relevant host compartments and specific bacterial structures able to trigger intestinal inflammation remain unclear. Here, we report that cell surface-associated lipoproteins and the enterococcal polysaccharide antigen, which are relevant for E. faecalis virulence in invertebrate infection models, but whose expression is minimally affected by the intestinal inflammatory milieu, exhibit colitogenic activity in a mouse model susceptible for chronic colitis. Bacterial lipoproteins trigger innate immune cell activation and are a critical prerequisite for E. faecalis-induced colitis. The enterococcal polysaccharide antigen mediates bacterial mucus penetration and adhesion to mucosal surfaces, promotes the formation of biofilm and contributes to E. faecalis colitogenic activity. Using E. faecalis as a model organism, we demonstrate that colitogenic activity of opportunistic pathogens can be assigned to specific bacterial structures, a finding that may help to identify the most essential steps in IBD-related microbe-host interactions.
Zdroje
1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59–65. doi: 10.1038/nature08821 20203603
2. Sava IG, Heikens E, Huebner J (2010) Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 16: 533–540.
3. Arias CA, Murray BE (2012) The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 10: 266–278. doi: 10.1038/nrmicro2761 22421879
4. Pinholt M, Ostergaard C, Arpi M, Bruun NE, Schønheyder HC, et al. (2014) Incidence, clinical characteristics and 30-day mortality of enterococcal bacteraemia in Denmark 2006–2009: a population-based cohort study. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 20: 145–151.
5. Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, et al. (2013) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010. Infect Control Hosp Epidemiol Off J Soc Hosp Epidemiol Am 34: 1–14.
6. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9: 313–323. doi: 10.1038/nri2515 19343057
7. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, et al. (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491: 119–124. doi: 10.1038/nature11582 23128233
8. Chassaing B, Darfeuille-Michaud A (2011) The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140: 1720–1728. doi: 10.1053/j.gastro.2011.01.054 21530738
9. Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577–594. doi: 10.1053/j.gastro.2007.11.059 18242222
10. Kostic AD, Xavier RJ, Gevers D (2014) The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146: 1489–1499. doi: 10.1053/j.gastro.2014.02.009 24560869
11. Shiga H, Kajiura T, Shinozaki J, Takagi S, Kinouchi Y, et al. (2012) Changes of faecal microbiota in patients with Crohn’s disease treated with an elemental diet and total parenteral nutrition. Dig Liver Dis Off J Ital Soc Gastroenterol Ital Assoc Study Liver. http://www.ncbi.nlm.nih.gov/pubmed/22622202. Accessed 25 June 2012.
12. Mondot S, Kang S, Furet JP, Aguirre de Carcer D, McSweeney C, et al. (2011) Highlighting new phylogenetic specificities of Crohn’s disease microbiota. Inflamm Bowel Dis 17: 185–192. doi: 10.1002/ibd.21436 20722058
13. Furrie E, Macfarlane S, Cummings JH, Macfarlane GT (2004) Systemic antibodies towards mucosal bacteria in ulcerative colitis and Crohn’s disease differentially activate the innate immune response. Gut 53: 91–98. 14684582
14. Fite A, Macfarlane S, Furrie E, Bahrami B, Cummings JH, et al. (2013) Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration. J Clin Microbiol 51: 849–856. doi: 10.1128/JCM.02574-12 23269735
15. Golińska E, Tomusiak A, Gosiewski T, Więcek G, Machul A, et al. (2013) Virulence factors of Enterococcus strains isolated from patients with inflammatory bowel disease. World J Gastroenterol WJG 19: 3562–3572. doi: 10.3748/wjg.v19.i23.3562 23801857
16. Barnett MPG, McNabb WC, Cookson AL, Zhu S, Davy M, et al. (2010) Changes in colon gene expression associated with increased colon inflammation in interleukin-10 gene-deficient mice inoculated with Enterococcus species. BMC Immunol 11: 39. doi: 10.1186/1471-2172-11-39 20630110
17. Balish E, Warner T (2002) Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 160: 2253–2257. 12057927
18. Kim SC, Tonkonogy SL, Albright CA, Tsang J, Balish EJ, et al. (2005) Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128: 891–906. 15825073
19. Ruiz PA, Shkoda A, Kim SC, Sartor RB, Haller D (2005) IL-10 gene-deficient mice lack TGF-beta/Smad signaling and fail to inhibit proinflammatory gene expression in intestinal epithelial cells after the colonization with colitogenic Enterococcus faecalis. J Immunol Baltim Md 1950 174: 2990–2999. 15728512
20. Steck N, Hoffmann M, Sava IG, Kim SC, Hahne H, et al. (2011) Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology 141: 959–971. doi: 10.1053/j.gastro.2011.05.035 21699778
21. Xu Y, Murray BE, Weinstock GM (1998) A Cluster of Genes Involved in Polysaccharide Biosynthesis from Enterococcus faecalis OG1RF. Infect Immun 66: 4313–4323. 9712783
22. Rigottier-Gois L, Madec C, Navickas A, Matos RC, Akary-Lepage E, et al. (2014) The Surface Rhamnopolysaccharide Epa of Enterococcus faecalis is a Key Determinant for Intestinal Colonization. J Infect Dis.
23. Geiss-Liebisch S, Rooijakkers SHM, Beczala A, Sanchez-Carballo P, Kruszynska K, et al. (2012) Secondary Cell Wall Polymers of Enterococcus faecalis Are Critical for Resistance to Complement Activation via Mannose-binding Lectin. J Biol Chem 287: 37769–37777. doi: 10.1074/jbc.M112.358283 22908219
24. Teng F, Singh KV, Bourgogne A, Zeng J, Murray BE (2009) Further characterization of the epa gene cluster and Epa polysaccharides of Enterococcus faecalis. Infect Immun 77: 3759–3767. doi: 10.1128/IAI.00149-09 19581393
25. Xu Y, Singh KV, Qin X, Murray BE, Weinstock GM (2000) Analysis of a Gene Cluster of Enterococcus faecalis Involved in Polysaccharide Biosynthesis. Infect Immun 68: 815–823. 10639451
26. Singh KV, Lewis RJ, Murray BE (2009) Importance of the epa locus of Enterococcus faecalis OG1RF in a mouse model of ascending urinary tract infection. J Infect Dis 200: 417–420. doi: 10.1086/600124 19545208
27. Zeng J, Teng F, Weinstock GM, Murray BE (2004) Translocation of Enterococcus faecalis strains across a monolayer of polarized human enterocyte-like T84 cells. J Clin Microbiol 42: 1149–1154. 15004067
28. Teng F, Jacques-Palaz KD, Weinstock GM, Murray BE (2002) Evidence that the enterococcal polysaccharide antigen gene (epa) cluster is widespread in Enterococcus faecalis and influences resistance to phagocytic killing of E. faecalis. Infect Immun 70: 2010–2015. 11895965
29. Prajsnar TK, Renshaw SA, Ogryzko NV, Foster SJ, Serror P, et al. (2013) Zebrafish as a novel vertebrate model to dissect enterococcal pathogenesis. Infect Immun 81: 4271–4279. doi: 10.1128/IAI.00976-13 24002065
30. Hutchings MI, Palmer T, Harrington DJ, Sutcliffe IC (2009) Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold ‘em, knowing when to fold ‘em. Trends Microbiol 17: 13–21. doi: 10.1016/j.tim.2008.10.001 19059780
31. Reffuveille F, Serror P, Chevalier S, Budin-Verneuil A, Ladjouzi R, et al. (2012) The prolipoprotein diacylglyceryl transferase (Lgt) of Enterococcus faecalis contributes to virulence. Microbiol Read Engl 158: 816–825.
32. Henneke P, Dramsi S, Mancuso G, Chraibi K, Pellegrini E, et al. (2008) Lipoproteins are critical TLR2 activating toxins in group B streptococcal sepsis. J Immunol Baltim Md 1950 180: 6149–6158. 18424736
33. Bubeck Wardenburg J, Williams WA, Missiakas D (2006) Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci U S A 103: 13831–13836. 16954184
34. Petit CM, Brown JR, Ingraham K, Bryant AP, Holmes DJ (2001) Lipid modification of prelipoproteins is dispensable for growth in vitro but essential for virulence in Streptococcus pneumoniae. FEMS Microbiol Lett 200: 229–233. 11425480
35. Wichgers Schreur PJ, Rebel JMJ, Smits MA, van Putten JPM, Smith HE (2011) Lgt processing is an essential step in Streptococcus suis lipoprotein mediated innate immune activation. PloS One 6: e22299. doi: 10.1371/journal.pone.0022299 21811583
36. Machata S, Tchatalbachev S, Mohamed W, Jänsch L, Hain T, et al. (2008) Lipoproteins of Listeria monocytogenes are critical for virulence and TLR2-mediated immune activation. J Immunol Baltim Md 1950 181: 2028–2035. 18641340
37. Zähringer U, Lindner B, Inamura S, Heine H, Alexander C (2008) TLR2—promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 213: 205–224. doi: 10.1016/j.imbio.2008.02.005 18406368
38. Hashimoto M, Tawaratsumida K, Kariya H, Kiyohara A, Suda Y, et al. (2006) Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J Immunol Baltim Md 1950 177: 3162–3169. 16920954
39. Singh S, Reese JM, Casanova-Torres AM, Goodrich-Blair H, Forst S (2014) Microbial Population Dynamics in the Hemolymph of Manduca sexta Infected with Xenorhabdus nematophila and the Entomopathogenic Nematode Steinernema carpocapsae. Appl Environ Microbiol 80: 4277–4285. doi: 10.1128/AEM.00768-14 24814780
40. Mason KL, Stepien TA, Blum JE, Holt JF, Labbe NH, et al. (2011) From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. mBio 2: e00065–00011. doi: 10.1128/mBio.00065-11 21586646
41. Hajishengallis G (2014) Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 35: 3–11. doi: 10.1016/j.it.2013.09.001 24269668
42. Yang I, Eibach D, Kops F, Brenneke B, Woltemate S, et al. (2013) Intestinal microbiota composition of interleukin-10 deficient C57BL/6J mice and susceptibility to Helicobacter hepaticus-induced colitis. PloS One 8: e70783. doi: 10.1371/journal.pone.0070783 23951007
43. Chow J, Mazmanian SK (2010) A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 7: 265–276. doi: 10.1016/j.chom.2010.03.004 20413095
44. Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, et al. (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487: 104–108. doi: 10.1038/nature11225 22722865
45. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, et al. (1998) Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterology 115: 1405–1413. 9834268
46. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, et al. (2004) Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology 127: 80–93. 15236175
47. Boudeau J, Glasser AL, Masseret E, Joly B, Darfeuille-Michaud A (1999) Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn’s disease. Infect Immun 67: 4499–4509. 10456892
48. Johansson MEV, Gustafsson JK, Holmén-Larsson J, Jabbar KS, Xia L, et al. (2013) Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut.
49. Macfarlane S, Furrie E, Cummings JH, Macfarlane GT (2004) Chemotaxonomic analysis of bacterial populations colonizing the rectal mucosa in patients with ulcerative colitis. Clin Infect Dis Off Publ Infect Dis Soc Am 38: 1690–1699.
50. Martinez-Medina M, Naves P, Blanco J, Aldeguer X, Blanco JE, et al. (2009) Biofilm formation as a novel phenotypic feature of adherent-invasive Escherichia coli (AIEC). BMC Microbiol 9: 202. doi: 10.1186/1471-2180-9-202 19772580
51. Reffuveille F, Leneveu C, Chevalier S, Auffray Y, Rincé A (2011) Lipoproteins of Enterococcus faecalis: bioinformatic identification, expression analysis and relation to virulence. Microbiol Read Engl 157: 3001–3013. doi: 10.1099/mic.0.053314-0 21903750
52. Reffuveille F, Connil N, Sanguinetti M, Posteraro B, Chevalier S, et al. (2012) Involvement of Peptidylprolyl cis/trans Isomerases in Enterococcus faecalis Virulence. Infect Immun 80: 1728–1735. doi: 10.1128/IAI.06251-11 22331431
53. Hancock LE, Gilmore MS (2002) The capsular polysaccharide of Enterococcus faecalis and its relationship to other polysaccharides in the cell wall. Proc Natl Acad Sci 99: 1574–1579. 11830672
54. Singh KV, Coque TM, Weinstock GM, Murray BE (1998) In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol Med Microbiol 21: 323–331. 9753005
55. Pierik M, Joossens S, Van Steen K, Van Schuerbeek N, Vlietinck R, et al. (2006) Toll-like receptor-1, -2, and -6 polymorphisms influence disease extension in inflammatory bowel diseases. Inflamm Bowel Dis 12: 1–8. 16374251
56. Podolsky DK, Gerken G, Eyking A, Cario E (2009) Colitis-associated variant of TLR2 causes impaired mucosal repair because of TFF3 deficiency. Gastroenterology 137: 209–220. doi: 10.1053/j.gastro.2009.03.007 19303021
57. Cario E, Gerken G, Podolsky DK (2007) Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 132: 1359–1374. 17408640
58. Szebeni B, Veres G, Dezsofi A, Rusai K, Vannay A, et al. (2008) Increased expression of Toll-like receptor (TLR) 2 and TLR4 in the colonic mucosa of children with inflammatory bowel disease. Clin Exp Immunol 151: 34–41. 17991289
59. Frolova L, Drastich P, Rossmann P, Klimesova K, Tlaskalova-Hogenova H (2008) Expression of Toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J Histochem Cytochem Off J Histochem Soc 56: 267–274.
60. Cantó E, Ricart E, Monfort D, González-Juan D, Balanzó J, et al. (2006) TNF alpha production to TLR2 ligands in active IBD patients. Clin Immunol Orlando Fla 119: 156–165. 16480927
61. Watanabe T, Kitani A, Murray PJ, Wakatsuki Y, Fuss IJ, et al. (2006) Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis. Immunity 25: 473–485. 16949315
62. Panesso D, Montealegre MC, Rincón S, Mojica MF, Rice LB, et al. (2011) The hylEfm gene in pHylEfm of Enterococcus faecium is not required in pathogenesis of murine peritonitis. BMC Microbiol 11: 20. doi: 10.1186/1471-2180-11-20 21266081
63. Kristich CJ, Chandler JR, Dunny GM (2007) Development of a host-genotype-independent counterselectable marker and a high-frequency conjugative delivery system and their use in genetic analysis of Enterococcus faecalis. Plasmid 57: 131–144. 16996131
64. Cieslewicz MJ, Kasper DL, Wang Y, Wessels MR (2001) Functional analysis in type Ia group B Streptococcus of a cluster of genes involved in extracellular polysaccharide production by diverse species of streptococci. J Biol Chem 276: 139–146. 11027683
65. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, et al. (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341: 1241214. doi: 10.1126/science.1241214 24009397
66. Gruber L, Kisling S, Lichti P, Martin F- P, May S, et al. (2013) High fat diet accelerates pathogenesis of murine Crohn’s disease-like ileitis independently of obesity. PloS One 8: e71661. doi: 10.1371/journal.pone.0071661 23977107
67. Theilacker C, Kropec A, Hammer F, Sava I, Wobser D, et al. (2012) Protection against Staphylococcus aureus by antibody to the polyglycerolphosphate backbone of heterologous lipoteichoic acid. J Infect Dis 205: 1076–1085. doi: 10.1093/infdis/jis022 22362863
68. Hufnagel M, Hancock LE, Koch S, Theilacker C, Gilmore MS, et al. (2004) Serological and genetic diversity of capsular polysaccharides in Enterococcus faecalis. J Clin Microbiol 42: 2548–2557. 15184433
69. Katakura K, Lee J, Rachmilewitz D, Li G, Eckmann L, et al. (2005) Toll-like receptor 9-induced type I IFN protects mice from experimental colitis. J Clin Invest 115: 695–702. 15765149
70. Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172: 762–770. 1688842
71. Stiernagle T (2006) Maintenance of C. elegans. WormBook Online Rev C Elegans Biol: 1–11.
72. Baldwin KM, Hakim RS (1987) Change of form of septate and gap junctions during development of the insect midgut. Tissue Cell 19: 549–558. 18620211
73. Cioffi M, Wolfersberger MG (1983) Isolation of separate apical, lateral and basal plasma membrane from cells of an insect epithelium. A procedure based on tissue organization and ultrastructure. Tissue Cell 15: 781–803. 6648956
74. Cioffi M (1979) The morphology and fine structure of the larval midgut of a moth (Manduca sexta) in relation to active ion transport. Tissue Cell 11: 467–479. 494237
75. Kanost MR, Jiang H, Yu X-Q (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 198: 97–105. 15199957
76. Brinkmann N, Martens R, Tebbe CC (2008) Origin and diversity of metabolically active gut bacteria from laboratory-bred larvae of Manduca sexta (Sphingidae, Lepidoptera, Insecta). Appl Environ Microbiol 74: 7189–7196. doi: 10.1128/AEM.01464-08 18849461
77. Van der Hoeven R, Betrabet G, Forst S (2008) Characterization of the gut bacterial community in Manduca sexta and effect of antibiotics on bacterial diversity and nematode reproduction. FEMS Microbiol Lett 286: 249–256. doi: 10.1111/j.1574-6968.2008.01277.x 18647359
78. Broderick NA, Raffa KF, Handelsman J (2006) Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci U S A 103: 15196–15199. 17005725
79. Eleftherianos I, ffrench-Constant RH, Clarke DJ, Dowling AJ, Reynolds SE (2010) Dissecting the immune response to the entomopathogen Photorhabdus. Trends Microbiol 18: 552–560. doi: 10.1016/j.tim.2010.09.006 21035345
80. Baldassarri L, Cecchini R, Bertuccini L, Ammendolia MG, Iosi F, et al. (2001) Enterococcus spp. produces slime and survives in rat peritoneal macrophages. Med Microbiol Immunol (Berl) 190: 113–120. 11827199
81. Deighton M, Borland R (1993) Regulation of slime production in Staphylococcus epidermidis by iron limitation. Infect Immun 61: 4473–4479. 8406839
82. Whitehead RH, Robinson PS, Williams JA, Bie W, Tyner AL, et al. (2008) Conditionally immortalized colonic epithelial cell line from a Ptk6 null mouse that polarizes and differentiates in vitro. J Gastroenterol Hepatol 23: 1119–1124. doi: 10.1111/j.1440-1746.2008.05308.x 18205771
83. Chassaing B, Darfeuille-Michaud A (2013) The δE Pathway Is Involved in Biofilm Formation by Crohn’s Disease-Associated Adherent-Invasive Escherichia coli. J Bacteriol 195: 76–84. doi: 10.1128/JB.01079-12 23104802
84. Gaspar F, Teixeira N, Rigottier-Gois L, Marujo P, Nielsen-LeRoux C, et al. (2009) Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE. Microbiology 155: 3564–3571. doi: 10.1099/mic.0.030775-0 19696101
85. Sifri CD, Mylonakis E, Singh KV, Qin X, Garsin DA, et al. (2002) Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70: 5647–5650. 12228293
86. Rigottier-Gois L, Alberti A, Houel A, Taly J-F, Palcy P, et al. (2011) Large-Scale Screening of a Targeted Enterococcus faecalis Mutant Library Identifies Envelope Fitness Factors. PLoS ONE 6: e29023. doi: 10.1371/journal.pone.0029023 22194979
87. Mohamed JA, Huang W, Nallapareddy SR, Teng F, Murray BE (2004) Influence of Origin of Isolates, Especially Endocarditis Isolates, and Various Genes on Biofilm Formation by Enterococcus faecalis. Infect Immun 72: 3658–3663. 15155680
88. Murray BE, Singh KV, Ross RP, Heath JD, Dunny GM, et al. (1993) Generation of restriction map of Enterococcus faecalis OG1 and investigation of growth requirements and regions encoding biosynthetic function. J Bacteriol 175: 5216–5223. 8349561
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 6
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- HIV Latency Is Established Directly and Early in Both Resting and Activated Primary CD4 T Cells
- A 21st Century Perspective of Poliovirus Replication
- Adenovirus Tales: From the Cell Surface to the Nuclear Pore Complex
- Battling Phages: How Bacteria Defend against Viral Attack