Host-specific induction of Escherichia coli fitness genes during human urinary tract infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 51, 2014, Pages 18327-18332

  Subashchandrabose, Sargurunathan ^a   Hazen, Tracy H ^b   Brumbaugh, Ariel R ^a   Himpsl, Stephanie D ^a   Smith, Sara N ^a   Ernst, Robert D ^a   Rasko, David A ^b   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Metal transport; RNA seq; UPEC; Uropathogenic E. coli; UTI

Indexed keywords

COPPER; CUPRIC ION; DRINKING WATER; NICKEL; POTASSIUM;

ADAPTATION; ANAEROBIC CAPACITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BLADDER; CONTROLLED STUDY; EXPERIMENTAL MODEL; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOST; HUMAN; ION TRANSPORT; MOUSE; NONHUMAN; POTASSIUM TRANSPORT; RNA SEQUENCE; URINARY TRACT INFECTION; URINE CULTURE; UROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MURINAE; MUS;

ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HUMANS; URINARY TRACT INFECTIONS;

EID: 84919905511     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1415959112     Document Type: Article

References (55)

1. Foxman B (2010) The epidemiology of urinary tract infection. Nat Rev Urol 7(12):653-660.
2. Litwin MS, et al.; Urologic Diseases in America Project (2005) Urologic diseases in America Project: Analytical methods and principal findings. J Urol 173(3):933-937.
3. Litwin MS, Saigal CS, Beerbohm EM (2005) The burden of urologic diseases in America. J Urol 173(4):1065-1066.
4. Gupta K, et al.; Infectious Diseases Society of America; European Society for Microbiology and Infectious Diseases (2011) 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 52(5):e103-e120.
5. Barber AE, Norton JP, Spivak AM, Mulvey MA (2013) Urinary tract infections: Current and emerging management strategies. Clin Infect Dis 57(5):719-724.
6. Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9(2):117-128.
7. Sivick KE, Mobley HL (2010) Waging war against uropathogenic Escherichia coli: Winning back the urinary tract. Infect Immun 78(2):568-585.
8. Alteri CJ, Mobley HL (2012) Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol 15(1):3-9.
9. Hannan TJ, et al. (2012) Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS Microbiol Rev 36(3):616-648.
10. Merrell DS, et al. (2002) Host-induced epidemic spread of the cholera bacterium. Nature 417(6889):642-645.
11. Hagan EC, Lloyd AL, Rasko DA, Faerber GJ, Mobley HL (2010) Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog 6(11):e1001187.
12. Subashchandrabose S, Hazen TH, Rasko DA, Mobley HL (2013) Draft genome sequences of five recent human uropathogenic Escherichia coli isolates. Pathog Dis 69(1):66-70.
13. Lloyd AL, Rasko DA, Mobley HL (2007) Defining genomic islands and uropathogenspecific genes in uropathogenic Escherichia coli. J Bacteriol 189(9):3532-3546.
14. Croucher NJ, Thomson NR (2010) Studying bacterial transcriptomes using RNA-seq. Curr Opin Microbiol 13(5):619-624.
15. Rasko DA, Myers GS, Ravel J (2005) Visualization of comparative genomic analyses by BLAST score ratio. BMC Bioinformatics 6:2.
16. Alteri CJ, Mobley HL (2007) Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine. Infect Immun 75(6):2679-2688.
17. Mobley HL, et al. (1990) Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: Role of hemolysin in some strains. Infect Immun 58(5):1281-1289.
18. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97(12):6640-6645.
19. Subashchandrabose S, Smith SN, Spurbeck RR, Kole MM, Mobley HL (2013) Genomewide detection of fitness genes in uropathogenic Escherichia coli during systemic infection. PLoS Pathog 9(12):e1003788.
20. Outten FW, Huffman DL, Hale JA, O'Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276(33):30670-30677.
21. Rowe JL, Starnes GL, Chivers PT (2005) Complex transcriptional control links NikABCDEdependent nickel transport with hydrogenase expression in Escherichia coli. J Bacteriol 187(18):6317-6323.
22. Laermann V, Ćudić E, Kipschull K, Zimmann P, Altendorf K (2013) The sensor kinase KdpD of Escherichia coli senses external K+. Mol Microbiol 88(6):1194-1204.
23. Thiennimitr P, et al. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci USA 108(42):17480-17485.
24. 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(1):298-305.
25. van der Ploeg JR, Eichhorn E, Leisinger T (2001) Sulfonate-sulfur metabolism and its regulation in Escherichia coli. Arch Microbiol 176(1-2):1-8.
26. Uria-Nickelsen MR, Leadbetter ER, Godchaux W, 3rd (1993) Sulphonate utilization by enteric bacteria. J Gen Microbiol 139(2):203-208.
27. Snyder JA, et al. (2004) Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72(11):6373-6381.
28. Mandlik A, et al. (2011) RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10(2):165-174.
29. Taveirne ME, Theriot CM, Livny J, DiRita VJ (2013) The complete Campylobacter jejuni transcriptome during colonization of a natural host determined by RNAseq. PloS one 8(8):e73586.
30. Bielecki P, et al. (2014) In vivo mRNA profiling of uropathogenic Escherichia coli from diverse phylogroups reveals common and group-specific gene expression profiles. MBio 5(4):e01075-14.
31. Willner D, et al. (2014) Single clinical isolates from acute uncomplicated urinary tract infections are representative of dominant in situ populations. MBio 5(2):e01064-e13.
32. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ (2007) Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 4(12):e329.
33. Cassat JE, Skaar EP (2013) Iron in infection and immunity. Cell Host Microbe 13(5):509-519.
34. Roos V, Klemm P (2006) Global gene expression profiling of the asymptomatic bacteriuria Escherichia coli strain 83972 in the human urinary tract. Infect Immun 74(6):3565-3575.
35. Hagan EC, Mobley HL (2007) Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection. Infect Immun 75(8):3941-3949.
36. Reigstad CS, Hultgren SJ, Gordon JI (2007) Functional genomic studies of uropathogenic Escherichia coli and host urothelial cells when intracellular bacterial communities are assembled. J Biol Chem 282(29):21259-21267.
37. Brumbaugh AR, Smith SN, Mobley HL (2013) Immunization with the yersiniabactin receptor, FyuA, protects against pyelonephritis in a murine model of urinary tract infection. Infect Immun 81(9):3309-3316.
38. Alteri CJ, Hagan EC, Sivick KE, Smith SN, Mobley HL (2009) Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog 5(9):e1000586.
39. Foxman B (2014) Urinary tract infection syndromes: Occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin North Am 28(1):1-13.
40. Mulvey MA, et al. (1998) Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282(5393):1494-1497.
41. Wiles TJ, Kulesus RR, Mulvey MA (2008) Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85(1):11-19.
42. White C, Lee J, Kambe T, Fritsche K, Petris MJ (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J Biol Chem 284(49):33949-33956.
43. Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP (2012) The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat Chem Biol 8(8):731-736.
44. Chaturvedi KS, et al. (2014) Cupric yersiniabactin is a virulence-associated superoxide dismutase mimic. ACS Chem Biol 9(2):551-561.
45. Tree JJ, et al. (2008) Trade-off between iron uptake and protection against oxidative stress: deletion of cueO promotes uropathogenic Escherichia coli virulence in a mouse model of urinary tract infection. J Bacteriol 190(20):6909-6912.
46. Nolan KJ, et al. (2002) In vivo behavior of a Helicobacter pylori SS1 nixA mutant with reduced urease activity. Infect Immun 70(2):685-691.
47. Hiron A, et al. (2010) A nickel ABC-transporter of Staphylococcus aureus is involved in urinary tract infection. Mol Microbiol 77(5):1246-1260.
48. Johnson DE, et al. (1993) Contribution of Proteus mirabilis urease to persistence, urolithiasis, and acute pyelonephritis in a mouse model of ascending urinary tract infection. Infect Immun 61(7):2748-2754.
49. Kulesus RR, Diaz-Perez K, Slechta ES, Eto DS, Mulvey MA (2008) Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76(7):3019-3026.
50. Johnson JR, Clabots C, Rosen H (2006) Effect of inactivation of the global oxidative stress regulator oxyR on the colonization ability of Escherichia coli O1:K1:H7 in a mouse model of ascending urinary tract infection. Infect Immun 74(1):461-468.
51. Hryckowian AJ, Welch RA (2013) RpoS contributes to phagocyte oxidase-mediated stress resistance during urinary tract infection by Escherichia coli CFT073. MBio 4(1):e00023-13.
52. Campbell EL, et al. (2014) Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity 40(1):66-77.
53. Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148(3):399-408.
54. Njoroge JW, Nguyen Y, Curtis MM, Moreira CG, Sperandio V (2012) Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. MBio 3(5):e00280-12.
55. Kendall MM, Gruber CC, Parker CT, Sperandio V (2012) Ethanolamine controls expression of genes encoding components involved in interkingdom signaling and virulence in enterohemorrhagic Escherichia coli O157:H7. MBio 3(3):e00050-12.