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Uropathogenic P and Type 1 Fimbriae Act in Synergy in a Living Host to Facilitate Renal Colonization Leading to Nephron Obstruction


The progression of a natural bacterial infection is a dynamic process influenced by the physiological characteristics of the target organ. Recent developments in live animal imaging allow for the study of the dynamic microbe-host interplay in real-time as the infection progresses within an organ of a live host. Here we used multiphoton microscopy-based live animal imaging, combined with advanced surgical procedures, to investigate the role of uropathogenic Escherichia coli (UPEC) attachment organelles P and Type 1 fimbriae in renal bacterial infection. A GFP+ expressing variant of UPEC strain CFT073 and genetically well-defined isogenic mutants were microinfused into rat glomerulus or proximal tubules. Within 2 h bacteria colonized along the flat squamous epithelium of the Bowman's capsule despite being exposed to the primary filtrate. When facing the challenge of the filtrate flow in the proximal tubule, the P and Type 1 fimbriae appeared to act in synergy to promote colonization. P fimbriae enhanced early colonization of the tubular epithelium, while Type 1 fimbriae mediated colonization of the center of the tubule via a mechanism believed to involve inter-bacterial binding and biofilm formation. The heterogeneous bacterial community within the tubule subsequently affected renal filtration leading to total obstruction of the nephron within 8 h. Our results reveal the importance of physiological factors such as filtration in determining bacterial colonization patterns, and demonstrate that the spatial resolution of an infectious niche can be as small as the center, or periphery, of a tubule lumen. Furthermore, our data show how secondary physiological injuries such as obstruction contribute to the full pathophysiology of pyelonephritis.


Vyšlo v časopise: Uropathogenic P and Type 1 Fimbriae Act in Synergy in a Living Host to Facilitate Renal Colonization Leading to Nephron Obstruction. PLoS Pathog 7(2): e32767. doi:10.1371/journal.ppat.1001298
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001298

Souhrn

The progression of a natural bacterial infection is a dynamic process influenced by the physiological characteristics of the target organ. Recent developments in live animal imaging allow for the study of the dynamic microbe-host interplay in real-time as the infection progresses within an organ of a live host. Here we used multiphoton microscopy-based live animal imaging, combined with advanced surgical procedures, to investigate the role of uropathogenic Escherichia coli (UPEC) attachment organelles P and Type 1 fimbriae in renal bacterial infection. A GFP+ expressing variant of UPEC strain CFT073 and genetically well-defined isogenic mutants were microinfused into rat glomerulus or proximal tubules. Within 2 h bacteria colonized along the flat squamous epithelium of the Bowman's capsule despite being exposed to the primary filtrate. When facing the challenge of the filtrate flow in the proximal tubule, the P and Type 1 fimbriae appeared to act in synergy to promote colonization. P fimbriae enhanced early colonization of the tubular epithelium, while Type 1 fimbriae mediated colonization of the center of the tubule via a mechanism believed to involve inter-bacterial binding and biofilm formation. The heterogeneous bacterial community within the tubule subsequently affected renal filtration leading to total obstruction of the nephron within 8 h. Our results reveal the importance of physiological factors such as filtration in determining bacterial colonization patterns, and demonstrate that the spatial resolution of an infectious niche can be as small as the center, or periphery, of a tubule lumen. Furthermore, our data show how secondary physiological injuries such as obstruction contribute to the full pathophysiology of pyelonephritis.


Zdroje

1. HillGS

1989 Renal Infection.

HillGS

Uropathology New York Churchill Livingstone 333 429

2. BowerJM

EtoDS

MulveyMA

2005 Covert operations of uropathogenic Escherichia coli within the urinary tract. Traffic 6 18 31

3. LaneMC

MobleyHL

2007 Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 72 19 25

4. MulveyMA

2002 Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4 257 271

5. MulveyMA

SchillingJD

MartinezJJ

HultgrenSJ

2000 Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci U S A 97 8829 8835

6. GodalyG

SvanborgC

2007 Urinary tract infections revisited. Kidney Int 71 721 723

7. WrightKJ

HultgrenSJ

2006 Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol 1 75 87

8. KalleniusG

MollbyR

SvensonSB

HelinI

HultbergH

1981 Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet 2 1369 1372

9. HagbergL

HullR

HullS

FalkowS

FreterR

1983 Contribution of adhesion to bacterial persistence in the mouse urinary tract. Infect Immun 40 265 272

10. MobleyHL

JarvisKG

ElwoodJP

WhittleDI

LockatellCV

1993 Isogenic P-fimbrial deletion mutants of pyelonephritogenic Escherichia coli: the role of alpha Gal(1-4) beta Gal binding in virulence of a wild-type strain. Mol Microbiol 10 143 155

11. RobertsJA

MarklundBI

IlverD

HaslamD

KaackMB

1994 The Gal(alpha 1-4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. Proc Natl Acad Sci U S A 91 11889 11893

12. TsengCC

HuangJJ

WangMC

WuAB

KoWC

2007 PapG II adhesin in the establishment and persistence of Escherichia coli infection in mouse kidneys. Kidney Int 71 764 770

13. HelmchenF

DenkW

2005 Deep tissue two-photon microscopy. Nat Methods 2 932 940

14. MelicanK

Richter-DahlforsA

2009 Real-time live imaging to study bacterial infections in vivo. Curr Opin Microbiol 12 31 36

15. PistonDW

1999 Imaging living cells and tissues by two-photon excitation microscopy. Trends Cell Biol 9 66 69

16. FrischknechtF

RenaudO

ShorteSL

2006 Imaging today's infectious animalcules. Curr Opin Microbiol 9 297 306

17. KonjufcaV

MillerMJ

2009 “Two-photon microscopy of host-pathogen interactions: acquiring a dynamic picture of infection in vivo”. Cell Microbiol 11 551 559

18. ManssonLE

MelicanK

MolitorisBA

Richter-DahlforsA

2007 Progression of bacterial infections studied in real time–novel perspectives provided by multiphoton microscopy. Cell Microbiol 9 2334 2343

19. ManssonLE

MelicanK

BoekelJ

SandovalRM

HautefortI

2007 Real-time studies of the progression of bacterial infections and immediate tissue responses in live animals. Cell Microbiol 9 413 424

20. MelicanK

BoekelJ

ManssonLE

SandovalRM

TannerGA

2008 Bacterial infection mediated mucosal signaling induces local renal ischemia as a defense against sepsis. Cell Microbiol 10 1987 1998

21. GorurS

CelikS

HakverdiS

AslantasO

ErdoganS

2008 Preventive effect of rolipram, a phosphodiesterase 4 enzyme inhibitor, on oxidative renal injury in acute ascending pyelonephritis model in rats. Urology 72 743 748

22. SerlachiusE

SundelinB

EklofAC

JahnkeM

LaestadiusA

1997 Pyelonephritis provokes growth retardation and apoptosis in infant rat renal cortex. Kidney Int 51 1855 1862

23. UhlenP

LaestadiusA

JahnukainenT

SoderblomT

BackhedF

2000 Alpha-haemolysin of uropathogenic E. coli induces Ca2+ oscillations in renal epithelial cells. Nature 405 694 697

24. BackhedF

AlsenB

RocheN

AngstromJ

von EulerA

2002 Identification of target tissue glycosphingolipid receptors for uropathogenic, F1C-fimbriated Escherichia coli and its role in mucosal inflammation. J Biol Chem 277 18198 18205

25. VercelloneA

StrattaP

1990 Historical review of concepts of pyelonephritis.

AmerioA

CoratelliP

MassrySG

Tubulo-Interstitial Nephropathies Proceedings of the 4th Bari Seminar in Nephrology Boston Kluwer Academic Publishers 197 205

26. WelchRA

BurlandV

PlunkettG3rd

RedfordP

RoeschP

2002 Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99 17020 17024

27. HautefortI

ProencaMJ

HintonJC

2003 Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ Microbiol 69 7480 7491

28. HoldenNJ

GallyDL

2004 Switches, cross-talk and memory in Escherichia coli adherence. J Med Microbiol 53 585 593

29. RhenM

MakelaPH

KorhonenK

1983 P-fimbriae of Escherichia coli are subjected to phase variation. FEMS Microbiol Lett 19 267 271

30. SnyderJA

HaugenBJ

LockatellCV

MaroncleN

HaganEC

2005 Coordinate expression of fimbriae in uropathogenic Escherichia coli. Infect Immun 73 7588 7596

31. LettingaG

Van VelsenAFM

HobmaSW

De ZeeuwW

KlapwijkA

1980 Use of the Upflow Sludge Blanket (USB) Reactor Concept for Biological Wastewater Treatment, Especially for Anaerobic Treatment. Biotechnol Bioeng 22 699 734

32. SonnenburgJL

AngenentLT

GordonJI

2004 Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 5 569 573

33. PrattLA

KolterR

1998 Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30 285 293

34. SchembriMA

KlemmP

2001 Biofilm formation in a hydrodynamic environment by novel fimh variants and ramifications for virulence. Infect Immun 69 1322 1328

35. ItoA

MayT

KawataK

OkabeS

2008 Significance of rpoS during maturation of Escherichia coli biofilms. Biotechnol Bioeng 99 1462 1471

36. AshworthSL

SandovalRM

TannerGA

MolitorisBA

2007 Two-photon microscopy: visualization of kidney dynamics. Kidney Int 72 416 421

37. CoombesJL

RobeyEA

2010 Dynamic imaging of host-pathogen interactions in vivo. Nat Rev Immunol 10 353 364

38. MelicanK

Richter-DahlforsA

2009 Multiphoton imaging of host-pathogen interactions. Biotechnol J 4 804 811

39. KummerliR

GriffinAS

WestSA

BucklingA

HarrisonF

2009 Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa. Proc Biol Sci 276 3531 3538

40. RatledgeC

DoverLG

2000 Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54 881 941

41. StenutzR

WeintraubA

WidmalmG

2006 The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol Rev 30 382 403

42. AndersonGG

PalermoJJ

SchillingJD

RothR

HeuserJ

2003 Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301 105 107

43. SticklerDJ

2008 Bacterial biofilms in patients with indwelling urinary catheters. Nat Clin Pract Urol 5 598 608

44. Le TrongI

AprikianP

KiddBA

Forero-SheltonM

TchesnokovaV

2010 Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting. Cell 141 645 655

45. SokurenkoEV

VogelV

ThomasWE

2008 Catch-bond mechanism of force-enhanced adhesion: counterintuitive, elusive, but … widespread? Cell Host Microbe 4 314 323

46. ThomasWE

NilssonLM

ForeroM

SokurenkoEV

VogelV

2004 Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Mol Microbiol 53 1545 1557

47. ThomasWE

TrintchinaE

ForeroM

VogelV

SokurenkoEV

2002 Bacterial adhesion to target cells enhanced by shear force. Cell 109 913 923

48. EssigM

FriedlanderG

2003 Shear-stress-responsive signal transduction mechanisms in renal proximal tubule cells. Curr Opin Nephrol Hypertens 12 31 34

49. RonaldLS

YakovenkoO

YazvenkoN

ChattopadhyayS

AprikianP

2008 Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 105 10937 10942

50. NilssonLM

ThomasWE

TrintchinaE

VogelV

SokurenkoEV

2006 Catch bond-mediated adhesion without a shear threshold: trimannose versus monomannose interactions with the FimH adhesin of Escherichia coli. J Biol Chem 281 16656 16663

51. Le BouguenecC

2005 Adhesins and invasins of pathogenic Escherichia coli. Int J Med Microbiol 295 471 478

52. TannerGA

1979 Effects of kidney tubule obstruction on glomerular function in rats. Am J Physiol 237 F379 385

53. TannerGA

KnoppLC

1986 Glomerular blood flow after single nephron obstruction in the rat kidney. Am J Physiol 250 F77 85

54. DatsenkoKA

WannerBL

2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97 6640 6645

55. KarowM

GeorgopoulosC

1992 Isolation and characterization of the Escherichia coli msbB gene, a multicopy suppressor of null mutations in the high-temperature requirement gene htrB. J Bacteriol 174 702 710

56. ClementsMO

ErikssonS

ThompsonA

LucchiniS

HintonJC

2002 Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc Natl Acad Sci U S A 99 8784 8789

57. RhenM

1985 Characterization of DNA fragments encoding fimbriae of the uropathogenic Escherichia coli strain KS71. J Gen Microbiol 131 571 580

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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