A shear stress micromodel of urinary tract infection by the Escherichia coli producing Dr adhesin - Publikacja - MOST Wiedzy


A shear stress micromodel of urinary tract infection by the Escherichia coli producing Dr adhesin


In this study, we established a dynamic micromodel of urinary tract infection to analyze the impact of UT-segment-specific urinary outflow on the persistence of E. coli colonization. We found that the adherence of Dr+ E. coli to bladder T24 transitional cells and type IV collagen is maximal at lowest shear stress and is reduced by any increase in flow velocity. The analyzed adherence was effective in the whole spectrum of physiological shear stress and was almost irreversible over the entire range of generated shear force. Once Dr+ E. coli bound to host cells or collagen, they did not detach even in the presence of elevated shear stress or of chloramphenicol, a competitive inhibitor of binding. Investigating the role of epithelial surface architecture, we showed that the presence of budding cells–a model microarchitectural obstacle–promotes colonization of the urinary tract by E. coli. We report a previously undescribed phenomenon of epithelial cell “rolling-shedding” colonization, in which the detached epithelial cells reattach to the underlying cell line through a layer of adherent Dr+ E. coli. This rolling-shedding colonization progressed continuously due to “refilling” induced by the flow-perturbing obstacle. The shear stress of fluid containing free-floating bacteria fueled the rolling, while providing an uninterrupted supply of new bacteria to be trapped by the rolling cell. The progressive rolling allows for transfer of briefly attached bacteria onto the underlying monolayer in a repeating cascading event.


  • 1 4


  • 1 3

    Web of Science

  • 1 2


Cytuj jako

Pełna treść

pobierz publikację
pobrano 26 razy
Wersja publikacji
Accepted albo Published Version
Creative Commons: CC-BY otwiera się w nowej karcie

Słowa kluczowe

Informacje szczegółowe

Publikacja w czasopiśmie
artykuły w czasopismach
Opublikowano w:
PLoS Pathogens nr 16, strony 1 - 32,
ISSN: 1553-7366
Rok wydania:
Opis bibliograficzny:
Zalewska-Piątek B., Olszewski M., Lipniacki T., Błoński S., Wieczór M., Bruździak P., Skwarska A., Nowicki B., Nowicki S., Piątek R.: A shear stress micromodel of urinary tract infection by the Escherichia coli producing Dr adhesin// PLoS Pathogens -Vol. 16,iss. 1 (2020), s.1-32
Cyfrowy identyfikator dokumentu elektronicznego (otwiera się w nowej karcie) 10.1371/journal.ppat.1008247
Bibliografia: test
  1. Stamm WE, Norrby SR. Urinary Tract Infections: Disease Panorama and Challenges. J Infect Dis. 2002; 183(S1): S1-4. otwiera się w nowej karcie
  2. Foxman B. The epidemiology of urinary tract infection. Nature Reviews Urology. 2010; 7: 653-660. https://doi.org/10.1038/nrurol.2010.190 PMID: 21139641 otwiera się w nowej karcie
  3. Foxman B. Urinary tract infection syndromes. Occurrence, recurrence, bacteriology, risk factors, and disease burden. Infectious Disease Clinics of North America. 2014; 28: 1-13. https://doi.org/10.1016/j. idc.2013.09.003 PMID: 24484571 otwiera się w nowej karcie
  4. Wurpel DJ, Beatson SA, Totsika M, Petty NK, Schembri MA. Chaperone-Usher Fimbriae of Escherichia coli. PLoS One. 2013; 8(1):e52835. https://doi.org/10.1371/journal.pone.0052835 PMID: 23382825 otwiera się w nowej karcie
  5. Zavyalov V, Zavialov A, Zav'Yalova G, Korpela T. Adhesive organelles of Gram-negative pathogens assembled with the classical chaperone/usher machinery: Structure and function from a clinical stand- point. FEMS Microbiology Reviews. 2010; 34: 317-378. https://doi.org/10.1111/j.1574-6976.2009. 00201.x PMID: 20070375 otwiera się w nowej karcie
  6. Geibel S, Waksman G. The molecular dissection of the chaperone-usher pathway. Biochimica et Bio- physica Acta-Molecular Cell Research. 2014; 1843: 1559-1567. otwiera się w nowej karcie
  7. Busch A, Phan G, Waksman G. Molecular mechanism of bacterial type 1 and P pili assembly. Philo- sophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences. 2015 Mar 6; 373(2036). pii: 20130153. https://doi.org/10.1098/rsta.2013.0153 otwiera się w nowej karcie
  8. Servin AL. Pathogenesis of human diffusely adhering Escherichia coli expressing Afa/Dr adhesins (Afa/ Dr DAEC): Current insights and future challenges. Clin Microbiol Rev. 2014; 27: 823-869. https://doi. org/10.1128/CMR.00036-14 PMID: 25278576 otwiera się w nowej karcie
  9. Anderson KL, Billington J, Pettigrew D, Cota E, Simpson P, Roversi P, et al. An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol Cell. 2004; 15: 647-657. https://doi.org/ 10.1016/j.molcel.2004.08.003 PMID: 15327779 otwiera się w nowej karcie
  10. Cota E, Jones C, Simpson P, Altroff H, Anderson KL, Du Merle L, et al. The solution structure of the invasive tip complex from Afa/Dr fibrils. Mol Microbiol. 2006; 62: 356-366. https://doi.org/10.1111/j. 1365-2958.2006.05375.x PMID: 16965519 otwiera się w nowej karcie
  11. Jȩ drzejczak R, Dauter Z, Dauter M, Piątek R, Zalewska B, Mró z M, et al. Structure of DraD invasin from uropathogenic Escherichia coli: A dimer with swapped β-tails. Acta Crystallogr Sect D Biol Crystallogr. 2006; 62: 157-164. otwiera się w nowej karcie
  12. Piątek R, Zalewska B, Kolaj O, Ferens M, Nowicki B, Kur J. Molecular aspects of biogenesis of Escheri- chia coli Dr Fimbriae: Characterization of DraB-DraE complexes. Infect Immun. 2005; 73: 135-145. https://doi.org/10.1128/IAI.73.1.135-145.2005 PMID: 15618148 otwiera się w nowej karcie
  13. Berger CN, Billker O, Meyer TF, Servin AL, Kansau I. Differential recognition of members of the carcino- embryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol Microbiol. 2004; 52: 963-983. https://doi.org/10.1111/j.1365-2958.2004.04033.x PMID: 15130118 otwiera się w nowej karcie
  14. Guignot J, Peiffer I, Bernet-Camard MF, Lublin DM, Carnoy C, Moseley SL, et al. Recruitment of CD55 and CD66e brush border-associated glycosylphosphatidylinositol-anchored proteins by members of the Afa/Dr diffusely adhering family of Escherichia coli that infect the human polarized intestinal Caco-2/ TC7 cells. Infect Immun. 2000; 68: 3554-3563. https://doi.org/10.1128/iai.68.6.3554-3563.2000 PMID: 10816511 otwiera się w nowej karcie
  15. Nowicki B, Moulds J, Hull R, Hull S. A hemagglutinin of uropathogenic Escherichia coli recognizes the Dr blood group antigen. Infect Immun. 1988; 56: 1057-1060. PMID: 2895740 otwiera się w nowej karcie
  16. Westerlund B, Kuusela P, Risteli J, Risteli L, Vartio T, Rauvala H, et al. The O75X adhesin of uropatho- genic Escherichia coli is a type IV collagen-binding protein. Mol Microbiol. 1989; 3: 329-337. https://doi. org/10.1111/j.1365-2958.1989.tb00178.x PMID: 2568575 otwiera się w nowej karcie
  17. Carnoy C, Moseley SL. Mutational analysis of receptor binding mediated by the Dr family of Escherichia coli adhesins. Mol Microbiol. 1997; 23: 365-379. https://doi.org/10.1046/j.1365-2958.1997.2231590.x PMID: 9044270 otwiera się w nowej karcie
  18. Korotkova N, Cota E, Lebedin Y, Monpouet S, Guignot J, Servin AL, et al. A subfamily of Dr adhesins of Escherichia coli bind independently to decay-accelerating factor and the N-domain of carcinoembryonic antigen. J Biol Chem. 2006; 281: 29120-29130. https://doi.org/10.1074/jbc.M605681200 PMID: 16882658 otwiera się w nowej karcie
  19. Pettigrew D, Anderson KL, Billington J, Cota E, Simpson P, Urvil P, et al. High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J Biol Chem. 2004; 279: 46851-46857. https://doi.org/10.1074/jbc.M409284200 PMID: 15331605 otwiera się w nowej karcie
  20. Sokurenko E V., Vogel V, Thomas WE. Catch-Bond Mechanism of Force-Enhanced Adhesion: Coun- terintuitive, Elusive, but . . . Widespread? Cell Host and Microbe. 2008; 4: 314-323. https://doi.org/10. 1016/j.chom.2008.09.005 PMID: 18854236 otwiera się w nowej karcie
  21. Thomas W. Catch Bonds in Adhesion. Annu Rev Biomed Eng. 2008; 10: 39-57. https://doi.org/10. 1146/annurev.bioeng.10.061807.160427 PMID: 18647111 otwiera się w nowej karcie
  22. Thomas WE, Vogel V, Sokurenko E. Biophysics of Catch Bonds. Annu Rev Biophys. 2008; 37: 399- 416. https://doi.org/10.1146/annurev.biophys.37.032807.125804 PMID: 18573088 otwiera się w nowej karcie
  23. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko E V. Bacterial adhesion to target cells enhanced by shear force. Cell. 2002; 109: 913-922. https://doi.org/10.1016/s0092-8674(02)00796-1 PMID: 12110187 otwiera się w nowej karcie
  24. Sauer MM, Jakob RP, Eras J, Baday S, Eriş D, Navarra G, et al. Catch-bond mechanism of the bacterial adhesin FimH. Nat Commun. 2016 Mar 7; 7:10738. https://doi.org/10.1038/ncomms10738 PMID: 26948702 otwiera się w nowej karcie
  25. Anderson BN, Ding AM, Nilsson LM, Kusuma K, Tchesnokova V, Vogel V, et al. Weak rolling adhesion enhances bacterial surface colonization. J Bacteriol. 2007; 189: 1794-1802. https://doi.org/10.1128/JB. 00899-06 PMID: 17189376 otwiera się w nowej karcie
  26. Nilsson LM, Thomas WE, Sokurenko E V., Vogel V. Elevated shear stress protects Escherichia coli cells adhering to surfaces via catch bonds from detachment by soluble inhibitors. Appl Environ Micro- biol. 2006; 72: 3005-3010. https://doi.org/10.1128/AEM.72.4.3005-3010.2006 PMID: 16598008 otwiera się w nowej karcie
  27. Nilsson LM, Thomas WE, Trintchina E, Vogel V, Sokurenko E V. Catch bond-mediated adhesion with- out a shear threshold: Trimannose versus monomannose interactions with the FimH adhesin of Escher- ichia coli. J Biol Chem. 2006; 281: 16656-16663. https://doi.org/10.1074/jbc.M511496200 PMID: 16624825 otwiera się w nowej karcie
  28. Thomas WE, Nilsson LM, Forero M, Sokurenko E V., Vogel V. Shear-dependent "stick-and-roll" adhe- sion of type 1 fimbriated Escherichia coli. Mol Microbiol. 2004; 53: 1545-1557. https://doi.org/10.1111/j. 1365-2958.2004.04226.x PMID: 15387828 otwiera się w nowej karcie
  29. Gounon P, Jouve M, Le Bouguénec C. Immunocytochemistry of the AfaE adhesin and AfaD invasin produced by pathogenic Escherichia coli strains during interaction of the bacteria with HeLa cells by high-resolution scanning electron microscopy. Microbes Infect. 2000; 2: 359-365. https://doi.org/10. 1016/s1286-4579(00)00331-2 PMID: 10817637 otwiera się w nowej karcie
  30. De Llano DG, Esteban-Fernández A, Sá nchez-Patá n F, Martín-Á lvarez PJ, Moreno-Arribas MV, Barto- lomé B. Anti-adhesive activity of cranberry phenolic compounds and their microbial-derived metabolites against uropathogenic escherichia coli in bladder epithelial cell cultures. Int J Mol Sci. 2015; 16: 12119- 12130. https://doi.org/10.3390/ijms160612119 PMID: 26023719 otwiera się w nowej karcie
  31. Iyer JK, Dickey A, Rouhani P, Kaul A, Govindaraju N, Singh RN, et al. Nanodiamonds facilitate killing of intracellular uropathogenic e. Coli in an in vitro model of urinary tract infection pathogenesis. PLoS One. 2018 Jan 11; 13(1):e0191020. https://doi.org/10.1371/journal.pone.0191020 PMID: 29324795 otwiera się w nowej karcie
  32. Hunstad DA, Justice SS, Hung CS, Lauer SR, Hultgren SJ. Suppression of bladder epithelial cytokine responses by uropathogenic Escherichia coli. Infect Immun. 2005; 73: 3999-4006. https://doi.org/10. 1128/IAI.73.7.3999-4006.2005 PMID: 15972487 otwiera się w nowej karcie
  33. Garcia MI, Gounon P, Courcoux P, Labigne A, Le Bougué nec C. The afimbrial adhesive sheath encoded by the afa-3 gene cluster of pathogenic Escherichia coli is composed of two adhesins. Mol Microbiol. 1996; 19: 683-693. https://doi.org/10.1046/j.1365-2958.1996.394935.x PMID: 8820639 otwiera się w nowej karcie
  34. Goluszko P, Popov V, Selvarangan R, Nowicki S, Pham T, Nowicki BJ. Dr Fimbriae Operon of Uro- pathogenic Escherichia coli Mediate Microtubule-Dependent Invasion to the HeLa Epithelial Cell Line. J Infect Dis. 2008; 176: 158-167. otwiera się w nowej karcie
  35. Aprikian P, Interlandi G, Kidd BA, Le Trong I, Tchesnokova V, Yakovenko O, et al. The bacterial fimbrial tip acts as a mechanical force sensor. PLoS Biol. 2011 May; 9(5):e1000617. https://doi.org/10.1371/ journal.pbio.1000617 PMID: 21572990 otwiera się w nowej karcie
  36. Spaulding CN, Klein RD, Schreiber HL, Janetka JW, Hultgren SJ. Precision antimicrobial therapeutics: The path of least resistance? npj Biofilms Microbiomes. 2018 Feb 27; 4:4. https://doi.org/10.1038/ s41522-018-0048-3 PMID: 29507749 otwiera się w nowej karcie
  37. Pettigrew DM, Roversi P, Davies SG, Russell AJ, Lea SM. A structural study of the interaction between the Dr haemagglutinin DraE and derivatives of chloramphenicol. Acta Crystallogr Sect D Biol Crystal- logr. 2009; 65: 513-522. otwiera się w nowej karcie
  38. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J, et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science. 1998; 282: 1494-1497. https://doi.org/10.1126/science.282.5393.1494 PMID: 9822381 otwiera się w nowej karcie
  39. Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ. Bad bugs and beleaguered bladders: Interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci. 2002; 97: 8829- 8835. otwiera się w nowej karcie
  40. Fukushi Y, Orikasa S, Kagayama M. An electron microscopic study of the interaction between vesical epithelium and E. coli. Invest Urol. 1979; 17: 61-68. PMID: 376485 otwiera się w nowej karcie
  41. McTaggart LA, Rigby RC, Elliott TSJ. The pathogenesis of urinary tract infections associated with Escherichia coli, Staphylococcus saprophyticus and S. epidermidis. J Med Microbiol. 1990; 32: 135- 141. https://doi.org/10.1099/00222615-32-2-135 PMID: 2192064 otwiera się w nowej karcie
  42. Durlofsky L, Brady JF, Bossis G. Dynamic Simulation of Hydrodynamically Interacting Particles. J Fluid Mech. 1987; 180: 21-49. otwiera się w nowej karcie
  43. Mysorekar IU, Hultgren SJ. Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci. 2006; 103: 14170-14175. https://doi.org/10.1073/pnas. 0602136103 PMID: 16968784 otwiera się w nowej karcie
  44. Wu J, Miao Y, Abraham SN. The multiple antibacterial activities of the bladder epithelium. Ann Transl Med. 2017 Jan; 5(2):35. https://doi.org/10.21037/atm.2016.12.71 PMID: 28217700 otwiera się w nowej karcie
  45. Piątek R, Bruździak P, Zalewska-Piątek B, Kur J, Stangret J. Preclusion of irreversible destruction of Dr adhesin structures by a high activation barrier for the unfolding stage of the fimbrial DraE subunit. Bio- chemistry. 2009; 48: 11807-11816. https://doi.org/10.1021/bi900920k PMID: 19891507 otwiera się w nowej karcie
  46. Piątek R, Bruździak P, Wojciechowski M, Zalewska-Piątek B, Kur J. The noncanonical disulfide bond as the important stabilizing element of the immunoglobulin fold of the Dr fimbrial DraE subunit. Biochem- istry. 2010; 49: 1460-1468. https://doi.org/10.1021/bi901896b PMID: 20082522 otwiera się w nowej karcie
  47. Pilipczuk J, Zalewska-Piątek B, Bruździak P, Czub J, Wieczór M, Olszewski M, et al. Role of the disul- fide bond in stabilizing and folding of the fimbrial protein DraE from uropathogenic Escherichia coli. J Biol Chem. 2017; 292: 16136-16149. https://doi.org/10.1074/jbc.M117.785477 PMID: 28739804 otwiera się w nowej karcie
  48. Nowicki B. Short consensus repeat-3 domain of recombinant decay-accelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction. J Exp Med. 2004; 178: 2115-2121. otwiera się w nowej karcie
  49. Pham TQ, Goluszko P, Popov V, Nowicki S, Nowicki BJ. Molecular cloning and characterization of Dr- II, a nonfimbrial adhesin-i-like adhesin isolated from gestational pyelonephritis-associated Escherichia coli that binds to decay-accelerating factor. Infect Immun. 1997; 65: 4309-4318. PMID: 9317041 otwiera się w nowej karcie
  50. Goldman AJ, Cox RG, Brenner H. Slow viscous motion of a sphere parallel to a plane wall-II Couette flow. Chem Eng Sci. 1967; 22: 653-660. otwiera się w nowej karcie
  51. Goluszko P, Selvarangan R, Nowicki BJ, Nowicki S, Hart A, Pawelczyk E, et al. Rapid receptor-cluster- ing assay to detect uropathogenic and diarrheal Escherichia coli isolates bearing adhesins of the Dr family. J Clin Microbiol. 2001; 39: 2317-2320. https://doi.org/10.1128/JCM.39.6.2317-2320.2001 PMID: 11376081 otwiera się w nowej karcie
  52. Goluszko P, Selvarangan R, Popov V, Pham T, Wen JW, Singhal J. Decay-accelerating factor and cyto- skeleton redistribution pattern in HeLa cells infected with recombinant Escherichia coli strains express- ing Dr family of adhesins. Infect Immun. 1999; 67: 3989-3997. PMID: 10417165 otwiera się w nowej karcie
  53. Hudault S, Spiller OB, Morgan BP, Servin AL. Human diffusely adhering Escherichia coli expressing Afa/Dr adhesins that use human CD55 (decay-accelerating factor) as a receptor does not bind the rodent and pig analogues of CD55. Infect Immun. 2004; 72: 4859-4863. https://doi.org/10.1128/IAI.72. 8.4859-4863.2004 PMID: 15271948 otwiera się w nowej karcie
  54. Nowicki B, Martens M, Hart A, Nowicki S. Gestational Age-Dependent Distribution of Escherichia coli Fimbriae in Pregnant Patients with Pyelonephritis. Ann N Y Acad Sci. 1994; 730: 290-291. https://doi. org/10.1111/j.1749-6632.1994.tb44268.x PMID: 7915894 otwiera się w nowej karcie
  55. Hart A, Nowicki BJ, Reisner B, Pawelczyk E, Goluszko P, Urvil P, et al. Ampicillin-Resistant Escherichia coli in Gestational Pyelonephritis: Increased Occurrence and Association with the Colonization Factor Dr Adhesin. J Infect Dis. 2002; 183: 1526-1529. otwiera się w nowej karcie
  56. Kaul AK, Kumar D, Nagamani M, Goluszko P, Nowicki S, Nowicki BJ. Rapid cyclic changes in density and accessibility of endometrial ligands for Escherichia coli Dr fimbriae. Infect Immun. 1996; 64: 611- 615. PMID: 8550215 otwiera się w nowej karcie
  57. Kaul A, Nowicki BJ, Martens MG, Goluszko P, Hart A, Nagamani M, et al. Decay-Accelerating Factor Is Expressed in the Human Endometrium and May Serve as the Attachment Ligand for Dr Pili of Escheri- chia coli. Am J Reprod Immunol. 1994; 32: 194-199. https://doi.org/10.1111/j.1600-0897.1994. tb01114.x PMID: 7533500 otwiera się w nowej karcie
  58. Pacheco LD, Hankins GD, Costantine MM, Anderson GD, Pawelczyk E, Nowicki S, et al. The role of human decay-accelerating factor in the pathogenesis of preterm labor. Am J Perinatol. 2011; 28: 565- 570. https://doi.org/10.1055/s-0031-1274510 PMID: 21380985 otwiera się w nowej karcie
  59. Fang L, Nowicki BJ, Urvil P, Goluszko P, Nowicki S, Young SL, et al. Epithelial Invasion by Escherichia coli Bearing Dr Fimbriae Is Controlled by Nitric Oxide-Regulated Expression of CD55. Infect Immun. 2004; 72: 2907-2917. https://doi.org/10.1128/IAI.72.5.2907-2914.2004 PMID: 15102803 otwiera się w nowej karcie
  60. Banadakoppa M, Goluszko P, Liebenthal D, Nowicki BJ, Nowicki S, Yallampalli C. PI3K/Akt pathway restricts epithelial adhesion of Dr+ Escherichia coli by down-regulating the expression of decay acceler- ating factor. Exp Biol Med. 2014; 239: 581-594. otwiera się w nowej karcie
  61. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: Epidemiology, mecha- nisms of infection and treatment options. Nature Reviews Microbiology. 2015; 13: 269-84. https://doi. org/10.1038/nrmicro3432 PMID: 25853778 otwiera się w nowej karcie
Źródła finansowania:
Politechnika Gdańska

wyświetlono 138 razy

Publikacje, które mogą cię zainteresować

Meta Tagi