Bacterial self-defence: How Escherichia coli evades serum killing

FEMS Microbiology Letters

Volumn 354, Issue 1, 2014, Pages 1-9

  Miajlovic, Helen ^a   Smith, Stephen G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Capsule; Colanic acid; Complement; Envelope stress regulators; Lipopolysaccharide; Outer membrane proteins

Indexed keywords

CATHELICIDIN; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C3B; COMPLEMENT MEMBRANE ATTACK COMPLEX; DEFENSIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; OUTER MEMBRANE PROTEIN A; OUTER MEMBRANE PROTEIN C;

ANTIBIOTIC RESISTANCE; BACTERIAL CAPSULE; BACTERIAL GENE; BACTERIAL MENINGITIS; BACTERIAL OUTER MEMBRANE; BACTERIAL SURVIVAL; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT DEPOSITION; COMPLEMENT LECTIN PATHWAY; CYTOKINE PRODUCTION; ESCHERICHIA COLI; HUMAN; IMMUNE EVASION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEPSIS; SERUM BACTERICIDAL ACTIVITY; ANIMAL; BLOOD; ESCHERICHIA COLI INFECTION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANIMALS; BLOOD BACTERICIDAL ACTIVITY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; IMMUNE EVASION;

EID: 84899983124     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12419     Document Type: Review

References (66)

1. Aguero ME, Aron L, DeLuca AG, Timmis KN & Cabello FC (1984) A plasmid-encoded outer membrane protein, TraT, enhances resistance of Escherichia coli to phagocytosis. Infect Immun 46: 740-746.
2. Barondess JJ & Beckwith J (1995) bor gene of phage lambda, involved in serum resistance, encodes a widely conserved outer membrane lipoprotein. J Bacteriol 177: 1247-1253.
3. Bhakdi S, Kuller G, Muhly M, Fromm S, Seibert G & Parrisius J (1987) Formation of transmural complement pores in serum-sensitive Escherichia coli. Infect Immun 55: 206-210.
4. Binns MM, Mayden J & Levine RP (1982) Further characterization of complement resistance conferred on Escherichia coli by the plasmid genes traT of R100 and iss of ColV, I-K94. Infect Immun 35: 654-659.
5. Bowdish DM, Davidson DJ & Hancock RE (2005) A re-evaluation of the role of host defence peptides in mammalian immunity. Curr Protein Pept Sci 6: 35-51.
6. Buckles EL, Wang X, Lane MC et al. (2009) Role of the K2 capsule in Escherichia coli urinary tract infection and serum resistance. J Infect Dis 199: 1689-1697.
7. Bugla-Ploskonska G, Kiersnowski A, Futoma-Koloch B & Doroszkiewicz W (2009) Killing of Gram-negative bacteria with normal human serum and normal bovine serum: use of lysozyme and complement proteins in the death of Salmonella strains O48. Microb Ecol 58: 276-289.
8. Burns SM & Hull SI (1998) Comparison of loss of serum resistance by defined lipopolysaccharide mutants and an acapsular mutant of uropathogenic Escherichia coli O75:K5. Infect Immun 66: 4244-4253.
9. Bury-Mone S, Nomane Y, Reymond N et al. (2009) Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5: e1000651.
10. Callewaert L & Michiels CW (2010) Lysozymes in the animal kingdom. J Biosci 35: 127-160.
11. Clarke DJ (2010) The Rcs phosphorelay: more than just a two-component pathway. Future Microbiol 5: 1173-1184.
12. Dankert JR (1989) Complement-mediated inhibition of function in complement-resistant Escherichia coli. J Immunol 142: 1591-1595.
13. Dankert JR & Esser AF (1986) Complement-mediated killing of Escherichia coli: dissipation of membrane potential by a C9-derived peptide. Biochemistry 25: 1094-1100.
14. Degousee N, Kelvin DJ, Geisslinger G et al. (2011) Group V phospholipase A2 in bone marrow-derived myeloid cells and bronchial epithelial cells promotes bacterial clearance after Escherichia coli pneumonia. J Biol Chem 286: 35650-35662.
15. Dennis EA, Cao J, Hsu YH, Magrioti V & Kokotos G (2011) Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem Rev 111: 6130-6185.
16. Donaldson DM, Roberts RR, Larsen HS & Tew JG (1974) Interrelationship between serum beta-lysin, lysozyme, and the antibody-complement system in killing Escherichia coli. Infect Immun 10: 657-666.
17. Elsbach P (1998) The bactericidal/permeability-increasing protein (BPI) in antibacterial host defense. J Leukoc Biol 64: 14-18.
18. Gaspar JA, Thomas JA, Marolda CL & Valvano MA (2000) Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the function of the TolA protein. Mol Microbiol 38: 262-275.
19. Goller CC & Seed PC (2010) High-throughput identification of chemical inhibitors of E. coli Group 2 capsule biogenesis as anti-virulence agents. PLoS One 5: e11642.
20. Grozdanov L, Zahringer U, Blum-Oehler G et al. (2002) A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. J Bacteriol 184: 5912-5925.
21. Hancock RE & Scott MG (2000) The role of antimicrobial peptides in animal defenses. P Natl Acad Sci USA 97: 8856-8861.
22. Jacobson SH, Ostenson CG, Tullus K & Brauner A (1992) Serum resistance in Escherichia coli strains causing acute pyelonephritis and bacteraemia. APMIS 100: 147-153.
23. Johnson JR (1991) Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4: 80-128.
24. Johnson TJ, Wannemuehler YM & Nolan LK (2008) Evolution of the iss gene in Escherichia coli. Appl Environ Microbiol 74: 2360-2369.
25. Lamarche MG, Dozois CM, Daigle F, Caza M, Curtiss R 3rd, Dubreuil JD & Harel J (2005) Inactivation of the pst system reduces the virulence of an avian pathogenic Escherichia coli O78 strain. Infect Immun 73: 4138-4145.
26. Levy O (2000) Antimicrobial proteins and peptides of blood: templates for novel antimicrobial agents. Blood 96: 2664-2672.
27. Levy O, Ooi CE, Weiss J, Lehrer RI & Elsbach P (1994) Individual and synergistic effects of rabbit granulocyte proteins on Escherichia coli. J Clin Invest 94: 672-682.
28. Leying H, Suerbaum S, Kroll HP, Stahl D & Opferkuch W (1990) The capsular polysaccharide is a major determinant of serum resistance in K-1-positive blood culture isolates of Escherichia coli. Infect Immun 58: 222-227.
29. Li G, Laturnus C, Ewers C & Wieler LH (2005) Identification of genes required for avian Escherichia coli septicemia by signature-tagged mutagenesis. Infect Immun 73: 2818-2827.
30. Liu YF, Yan JJ, Lei HY, Teng CH, Wang MC, Tseng CC & Wu JJ (2012) Loss of outer membrane protein C in Escherichia coli contributes to both antibiotic resistance and escaping antibody-dependent bactericidal activity. Infect Immun 80: 1815-1822.
31. Lloubes R, Cascales E, Walburger A, Bouveret E, Lazdunski C, Bernadac A & Journet L (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152: 523-529.
32. Maisetta G, Di Luca M, Esin S et al. (2008) Evaluation of the inhibitory effects of human serum components on bactericidal activity of human beta defensin 3. Peptides 29: 1-6.
33. Maruvada R & Kim KS (2011) Extracellular loops of the Eschericia coli outer membrane protein A contribute to the pathogenesis of meningitis. J Infect Dis 203: 131-140.
34. Marx G & Reinhart K (2008) Urosepsis: from the intensive care viewpoint. Int J Antimicrob Agents 31(suppl 1): S79-S84.
35. Miajlovic H, Cooke NM, Moran GP, Rogers TR & Smith SG (2014) Response of extraintestinal pathogenic Escherichia coli to human serum reveals a protective role for Rcs-regulated exopolysaccharide colanic acid. Infect Immun 82: 298-305.
36. Mittal R, Krishnan S, Gonzalez-Gomez I & Prasadarao NV (2011) Deciphering the roles of outer membrane protein A extracellular loops in the pathogenesis of Escherichia coli K1 meningitis. J Biol Chem 286: 2183-2193.
37. Noah JW, Ananthan S, Evans CW et al. (2010a) 3-(2, 6-difluorobenzamido)-5-(4-ethoxyphenyl) thiophene-2-carboxylic acid inhibits. E. coli UT189 bacterial capsule biogenesis. Probe Reports from the NIH Molecular Libraries Program, Bethesda, MD.
38. Noah JW, Ananthan S, Evans CW et al. (2010b) N-(pyridin-4-yl)benzo[d]thiazole-6-carboxamide inhibits E. coli UT189 bacterial capsule biogenesis. Probe Reports from the NIH Molecular Libraries Program, Bethesda, MD.
39. O'Hara AM, Moran AP, Wurzner R & Orren A (2001) Complement-mediated lipopolysaccharide release and outer membrane damage in Escherichia coli J5: requirement for C9. Immunology 102: 365-372.
40. Opal S, Cross A & Gemski P (1982) K antigen and serum sensitivity of rough Escherichia coli. Infect Immun 37: 956-960.
41. Phan MD, Peters KM, Sarkar S et al. (2013) The serum resistome of a globally disseminated multidrug resistant uropathogenic clone. PLoS Genet 9: e1003834.
42. Pramoonjago P, Kaneko M, Kinoshita T et al. (1992) Role of TraT protein, an anticomplementary protein produced in Escherichia coli by R100 factor, in serum resistance. J Immunol 148: 827-836.
43. Prasadarao NV, Blom AM, Villoutreix BO & Linsangan LC (2002) A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1. J Immunol 169: 6352-6360.
44. Rautemaa R, Jarvis GA, Marnila P & Meri S (1998) Acquired resistance of Escherichia coli to complement lysis by binding of glycophosphoinositol-anchored protectin (CD59). Infect Immun 66: 1928-1933.
45. Rhodius VA, Suh WC, Nonaka G, West J & Gross CA (2006) Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4: e2.
46. Rittirsch D, Flierl MA & Ward PA (2008) Harmful molecular mechanisms in sepsis. Nat Rev Immunol 8: 776-787.
47. Russo TA & Johnson JR (2003) Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5: 449-456.
48. Russo TA, Moffitt MC, Hammer CH & Frank MM (1993) TnphoA-mediated disruption of K54 capsular polysaccharide genes in Escherichia coli confers serum sensitivity. Infect Immun 61: 3578-3582.
49. Sansano M Jr, Reynard AM & Cunningham RK (1985) Inhibition of serum bactericidal reaction by lipopolysaccharide. Infect Immun 48: 759-762.
50. Sarma JV & Ward PA (2011) The complement system. Cell Tissue Res 343: 227-235.
51. Schneider G, Dobrindt U, Bruggemann H et al. (2004) The pathogenicity island-associated K15 capsule determinant exhibits a novel genetic structure and correlates with virulence in uropathogenic Escherichia coli strain 536. Infect Immun 72: 5993-6001.
52. Siegfried L, Puzova H, Kmetova M & Kerestesova A (1992) Killing of alpha-haemolytic and non-haemolytic Escherichia coli strains in human serum and polymorphonuclear leucocytes. J Med Microbiol 37: 3-7.
53. Smith SG, Mahon V, Lambert MA & Fagan RP (2007) A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett 273: 1-11.
54. Snyder JA, Haugen BJ, Buckles EL et al. (2004) Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72: 6373-6381.
55. Subashchandrabose S, Smith SN, Spurbeck RR, Kole MM & Mobley HL (2013) Genome-wide detection of fitness genes in uropathogenic Escherichia coli during systemic infection. PLoS Pathog 9: e1003788.
56. Sukupolvi S & O'Connor D (1987) Amino acid alterations in a hydrophobic region of the TraT protein of R6-5 increase the outer membrane permeability of enteric bacteria. Mol Gen Genet 210: 178-180.
57. Taylor PW & Kroll HP (1984) Interaction of human complement proteins with serum-sensitive and serum-resistant strains of Escherichia coli. Mol Immunol 21: 609-620.
58. Taylor PW & Robinson MK (1980) Determinants that increase the serum resistance of Escherichia coli. Infect Immun 29: 278-280.
59. Tseng YT, Wang SW, Kim KS et al. (2012) NlpI facilitates deposition of C4 bp on Escherichia coli by blocking classical complement-mediated killing, which results in high-level bacteremia. Infect Immun 80: 3669-3678.
60. Ulett GC, Totsika M, Schaale K, Carey AJ, Sweet MJ & Schembri MA (2013) Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection. Curr Opin Microbiol 16: 100-107.
61. Vanderkelen L, Ons E, Van Herreweghe JM, Callewaert L, Goddeeris BM & Michiels CW (2012) Role of lysozyme inhibitors in the virulence of avian pathogenic Escherichia coli. PLoS One 7: e45954.
62. Vogt SL & Raivio TL (2012) Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol Lett 326: 2-11.
63. Wang CY, Wang SW, Huang WC et al. (2012) Prc contributes to Escherichia coli evasion of classical complement-mediated serum killing. Infect Immun 80: 3399-3409.
64. Weiser JN & Gotschlich EC (1991) Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect Immun 59: 2252-2258.
65. Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.
66. Wooster DG, Maruvada R, Blom AM & Prasadarao NV (2006) Logarithmic phase Escherichia coli K1 efficiently avoids serum killing by promoting C4bp-mediated C3b and C4b degradation. Immunology 117: 482-493.