Home LiteratureArticle Details
PMID: 23798537 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Immunization with the yersiniabactin receptor, FyuA, protects against pyelonephritis in a murine model of urinary tract infection.

Infection and immunity ·Vol. 81 ·No. 9 ·2013-09-00 ·Pages 3309-16

Brumbaugh AR, Smith SN, Mobley HL

Abstract

Urinary tract infections (UTI) are common and represent a substantial economic and public health burden. Roughly 80% of these infections are caused by a heterogeneous group of uropathogenic Escherichia coli (UPEC) strains. Antibiotics are standard therapy for UTI, but a rise in antibiotic resistance has complicated treatment, making the development of a UTI vaccine more urgent. Iron receptors are a promising new class of vaccine targets for UTI, as UPEC require iron to colonize the iron-limited host urinary tract and genes encoding iron acquisition systems are highly expressed during infection. Previously, three of six UPEC siderophore and heme receptors were identified as vaccine candidates by intranasal immunization in a murine model of ascending UTI. To complete the assessment of iron receptors as vaccine candidates, an additional six UPEC iron receptors were evaluated. Of the six vaccine candidates tested in this study (FyuA, FitA, IroN, the gene product of the CFT073 locus c0294, and two truncated derivatives of ChuA), only FyuA provided significant protection (P = 0.0018) against UPEC colonization. Intranasal immunization induced a robust and long-lived humoral immune response. In addition, the levels of FyuA-specific serum IgG correlated with bacterial loads in the kidneys [Spearman's rank correlation coefficient ρ(14) = -0.72, P = 0.0018], providing a surrogate of protection. FyuA is the fourth UPEC iron receptor to be identified from our screens, in addition to IutA, Hma, and IreA, which were previously demonstrated to elicit protection against UPEC challenge. Together, these iron receptor antigens will facilitate the development of a broadly protective, multivalent UTI vaccine to effectively target diverse strains of UPEC.

MeSH Terms
Administration, Intranasal Animals Antibodies, Bacterial/immunology Antigens, Bacterial/immunology Escherichia coli/immunology Escherichia coli Infections/immunology,microbiology,urine Escherichia coli Proteins/immunology Female Immunity, Humoral/immunology Immunization/methods Immunoglobulin A/immunology,urine Immunoglobulin G/immunology Iron/immunology Mice Mice, Inbred CBA Phenols/immunology Pyelonephritis/immunology,microbiology,prevention & control Receptors, Cell Surface/immunology Siderophores/immunology Thiazoles/immunology Urinary Tract Infections/immunology,microbiology,urine Uropathogenic Escherichia coli/immunology Vaccination/methods
Chemicals
Antibodies, Bacterial Antigens, Bacterial Escherichia coli Proteins Immunoglobulin A Immunoglobulin G Phenols Receptors, Cell Surface Siderophores Thiazoles heme receptor yersiniabactin Iron
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Brumbaugh Ariel R
Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan, USA.
Smith Sara N
Mobley Harry L T
References (54)
54 references, click to expand
  1. The ARESC study: an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections.
    Int J Antimicrob Agents. 2009 Nov;34(5):407-13 PMID: 19505803
  2. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains.
    Infect Immun. 1990 May;58(5):1281-9 PMID: 2182540
  3. National Hospital Discharge Survey: 2007 summary.
    Natl Health Stat Report. 2010 Oct 26;(29):1-20, 24 PMID: 21086860
  4. Uropathogenicity in rats and mice of Providencia stuartii from long-term catheterized patients.
    J Urol. 1987 Sep;138(3):632-5 PMID: 3625871
  5. Recurrent urinary tract infections in women: diagnosis and management.
    Am Fam Physician. 2010 Sep 15;82(6):638-43 PMID: 20842992
  6. Ambulatory medical care utilization estimates for 2007.
    Vital Health Stat 13. 2011 Apr;(169):1-38 PMID: 21614897
  7. The yersiniabactin transport system is critical for the pathogenesis of bubonic and pneumonic plague.
    Infect Immun. 2010 May;78(5):2045-52 PMID: 20160020
  8. A multiepitope subunit vaccine conveys protection against extraintestinal pathogenic Escherichia coli in mice.
    Infect Immun. 2010 Aug;78(8):3432-42 PMID: 20498257
  9. Molecular epidemiology and phylogenetic distribution of the Escherichia coli pks genomic island.
    J Clin Microbiol. 2008 Dec;46(12):3906-11 PMID: 18945841
  10. Extraintestinal isolates of Escherichia coli: identification and prospects for vaccine development.
    Expert Rev Vaccines. 2006 Feb;5(1):45-54 PMID: 16451107
  11. Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection.
    Infect Immun. 2007 Aug;75(8):3941-9 PMID: 17517861
  12. An "omics" approach to uropathogenic Escherichia coli vaccinology.
    Trends Microbiol. 2009 Oct;17(10):431-2 PMID: 19758805
  13. Yersinia high-pathogenicity island contributes to virulence in Escherichia coli causing extraintestinal infections.
    Infect Immun. 2002 Sep;70(9):5335-7 PMID: 12183596
  14. Urologic diseases in America Project: analytical methods and principal findings.
    J Urol. 2005 Mar;173(3):933-7 PMID: 15711342
  15. Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies.
    J Exp Med. 2008 Jan 21;205(1):117-31 PMID: 18166586
  16. Identification of in vivo-induced antigens including an RTX family exoprotein required for uropathogenic Escherichia coli virulence.
    Infect Immun. 2011 Jun;79(6):2335-44 PMID: 21422188
  17. Risk factors for second urinary tract infection among college women.
    Am J Epidemiol. 2000 Jun 15;151(12):1194-205 PMID: 10905532
  18. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing.
    Science. 2000 Mar 10;287(5459):1816-20 PMID: 10710308
  19. Identification of a common immune signature in murine and human systemic Salmonellosis.
    Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):4998-5003 PMID: 22331879
  20. Escherichia coli global gene expression in urine from women with urinary tract infection.
    PLoS Pathog. 2010 Nov 11;6(11):e1001187 PMID: 21085611
  21. Extended virulence genotypes and phylogenetic background of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis.
    J Infect Dis. 2005 Jan 1;191(1):46-50 PMID: 15593002
  22. Antibiotic resistance and pyelonephritis.
    Clin Infect Dis. 2007 Aug 1;45(3):281-3 PMID: 17599304
  23. Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract.
    Infect Immun. 2012 Dec;80(12):4115-22 PMID: 22966046
  24. Virulence factors in Escherichia coli urinary tract infection.
    Clin Microbiol Rev. 1991 Jan;4(1):80-128 PMID: 1672263
  25. Identification of uropathogenic Escherichia coli surface proteins by shotgun proteomics.
    J Microbiol Methods. 2009 Aug;78(2):131-5 PMID: 19426766
  26. The immortality of humoral immunity.
    Immunol Rev. 2010 Jul;236:139-50 PMID: 20636814
  27. Quantitative metabolomics reveals an epigenetic blueprint for iron acquisition in uropathogenic Escherichia coli.
    PLoS Pathog. 2009 Feb;5(2):e1000305 PMID: 19229321
  28. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5977-82 PMID: 16585510
  29. Antibiotherapy and pathogenesis of uncomplicated UTI: difficult relationships.
    J Appl Microbiol. 2009 Jun;106(6):1779-91 PMID: 19210569
  30. Spontaneous deletions and flanking regions of the chromosomally inherited hemolysin determinant of an Escherichia coli O6 strain.
    J Bacteriol. 1983 Jun;154(3):1145-52 PMID: 6343344
  31. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: A 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases.
    Clin Infect Dis. 2011 Mar 1;52(5):e103-20 PMID: 21292654
  32. Complicated urinary tract infection in adults.
    Can J Infect Dis Med Microbiol. 2005 Nov;16(6):349-60 PMID: 18159518
  33. Susceptibility patterns of orally administered antimicrobials among urinary tract infection pathogens from hospitalized patients in North America: comparison report to Europe and Latin America. Results from the SENTRY Antimicrobial Surveillance Program (2000).
    Diagn Microbiol Infect Dis. 2003 Apr;45(4):295-301 PMID: 12730002
  34. Targeting virulence traits: potential strategies to combat extraintestinal pathogenic E. coli infections.
    Curr Opin Microbiol. 2008 Oct;11(5):409-13 PMID: 18824126
  35. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs.
    Am J Med. 2002 Jul 8;113 Suppl 1A:5S-13S PMID: 12113866
  36. Diagnosis and management of uncomplicated urinary tract infections.
    Am Fam Physician. 2005 Aug 1;72(3):451-6 PMID: 16100859
  37. Transcriptome of uropathogenic Escherichia coli during urinary tract infection.
    Infect Immun. 2004 Nov;72(11):6373-81 PMID: 15501767
  38. Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli.
    J Bacteriol. 2007 May;189(9):3532-46 PMID: 17351047
  39. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection.
    Infect Immun. 2011 Mar;79(3):1225-35 PMID: 21220482
  40. Correlates of protection induced by vaccination.
    Clin Vaccine Immunol. 2010 Jul;17(7):1055-65 PMID: 20463105
  41. The epidemiology of urinary tract infection.
    Nat Rev Urol. 2010 Dec;7(12):653-60 PMID: 21139641
  42. Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine.
    Infect Immun. 2007 Jun;75(6):2679-88 PMID: 17513849
  43. Yersiniabactin is a virulence factor for Klebsiella pneumoniae during pulmonary infection.
    Infect Immun. 2007 Mar;75(3):1463-72 PMID: 17220312
  44. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli.
    Proc Natl Acad Sci U S A. 2010 May 18;107(20):9072-7 PMID: 20439758
  45. Mucosal immunization with iron receptor antigens protects against urinary tract infection.
    PLoS Pathog. 2009 Sep;5(9):e1000586 PMID: 19806177
  46. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007.
    Infect Control Hosp Epidemiol. 2008 Nov;29(11):996-1011 PMID: 18947320
  47. Emerging bacterial pathogens. Preface.
    Contrib Microbiol. 2001;8:XI-XIV PMID: 11764741
  48. Ambulatory medical care utilization estimates for 2006.
    Natl Health Stat Report. 2008 Aug 6;(8):1-29 PMID: 18958997
  49. Identification of candidates for a subunit vaccine against extraintestinal pathogenic Escherichia coli.
    Infect Immun. 2007 Apr;75(4):1916-25 PMID: 17145948
  50. Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs.
    Infect Dis Clin North Am. 2003 Jun;17(2):227-41 PMID: 12848468
  51. Antibiotic resistance in Escherichia coli outpatient urinary isolates: final results from the North American Urinary Tract Infection Collaborative Alliance (NAUTICA).
    Int J Antimicrob Agents. 2006 Jun;27(6):468-75 PMID: 16713191
  52. The Siderophore receptor IroN of extraintestinal pathogenic Escherichia coli is a potential vaccine candidate.
    Infect Immun. 2003 Dec;71(12):7164-9 PMID: 14638809
  53. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract.
    Mol Microbiol. 2002 Aug;45(4):1079-93 PMID: 12180926
  54. Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine.
    Expert Rev Vaccines. 2012 Jun;11(6):663-76 PMID: 22873125
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
1098-5522
Published
2013-09-00
Epub
2013-00-24
Pages
3309-16
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC3754202
Subset
IM
Grants
NIAID NIH HHS · R01 AI059722 · United States
NIAID NIH HHS · AI43365 · United States
NIAID NIH HHS · AI059722 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com