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
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
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
2007 Progression of bacterial infections studied in real time–novel perspectives provided by multiphoton microscopy. Cell Microbiol 9 2334 2343
19. ManssonLE
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
ManssonLE
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
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
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
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
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
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
2004 Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Mol Microbiol 53 1545 1557
47. ThomasWE
TrintchinaE
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
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
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
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
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
