Trimeric Autotransporter Adhesin-dependent Adherence of Bartonella Henselae, Bartonella Quintana, and Yersinia Enterocolitica to Matrix Components and Endothelial Cells Under Static and Dynamic Flow Conditions

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2011 May 4

PMID 21536788

Citations 35

Authors

Niklas F Muller

Patrick O Kaiser

Dirk Linke

Heinz Schwarz

Tanja Riess

Andrea Schafer

Johannes A Eble

Volkhard A J Kempf

Affiliations

Soon will be listed here.

Abstract

Trimeric autotransporter adhesins (TAAs) are important virulence factors of Gram-negative bacteria responsible for adherence to extracellular matrix (ECM) and host cells. Here, we analyzed three different TAAs (Bartonella adhesin A [BadA] of Bartonella henselae, variably expressed outer membrane proteins [Vomps] of Bartonella quintana, and Yersinia adhesin A [YadA] of Yersinia enterocolitica) for mediating bacterial adherence to ECM and endothelial cells. Using static (cell culture vials) and dynamic (capillary flow chambers) experimental settings, adherence of wild-type bacteria and of the respective TAA-negative strains was analyzed. Under static conditions, ECM adherence of B. henselae, B. quintana, and Y. enterocolitica was strongly dependent on the expression of their particular TAAs. YadA of Y. enterocolitica did not mediate bacterial binding to plasma or cellular fibronectin under either static or dynamic conditions. TAA-dependent host cell adherence appeared more significant under dynamic conditions although the total number of bound bacteria was diminished compared to the number under static conditions. Dynamic models expand the methodology to perform bacterial adherence experiments under more realistic, bloodstream-like conditions and allow dissection of the biological role of TAAs in ECM and host cell adherence under static and dynamic conditions.

Citing Articles

Comparison of transcriptomic profiles between intracellular and extracellular Bartonella henselae.

Gadila S, Caskey J, Breitschwerdt E, Maggi R, Embers M Commun Biol. 2025; 8(1):143.

PMID: 39881203 PMC: 11779821. DOI: 10.1038/s42003-025-07535-9.

Differential vasoproliferative traits of strains associated with autotransporter BafA variants.

Kondo Y, Suzuki M, Sato S, Maruyama S, Sei A, Ma X Microbiol Spectr. 2024; 13(1):e0192524.

PMID: 39611834 PMC: 11705867. DOI: 10.1128/spectrum.01925-24.

The Trimeric Autotransporter Adhesin SadA from spp. as a Novel Bacterial Surface Display System.

Sang S, Song W, Lu L, Ou Q, Guan Y, Tao H Vaccines (Basel). 2024; 12(4).

PMID: 38675781 PMC: 11054257. DOI: 10.3390/vaccines12040399.

Adhesion preference of the sticky bacterium sp. Tol 5.

Yoshimoto S, Ishii S, Kawashiri A, Matsushita T, Linke D, Gottig S Front Bioeng Biotechnol. 2024; 12:1342418.

PMID: 38375452 PMC: 10875045. DOI: 10.3389/fbioe.2024.1342418.

Two novel (sub)species isolated from edible dormice (): hints of cultivation stress-induced genomic changes.

Bartos O, Klimesova B, Volfova K, Chmel M, Dresler J, Pajer P Front Microbiol. 2023; 14:1289671.

PMID: 38033559 PMC: 10684924. DOI: 10.3389/fmicb.2023.1289671.

References

Bolin I, Norlander L, Wolf-Watz H . Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun. 1982; 37(2):506-12. PMC: 347563. DOI: 10.1128/iai.37.2.506-512.1982. View

Drancourt M, Birtles R, Chaumentin G, Vandenesch F, Etienne J, Raoult D . New serotype of Bartonella henselae in endocarditis and cat-scratch disease. Lancet. 1996; 347(8999):441-3. DOI: 10.1016/s0140-6736(96)90012-4. View

Skurnik M, Bolin I, Heikkinen H, PIHA S, Wolf-Watz H . Virulence plasmid-associated autoagglutination in Yersinia spp. J Bacteriol. 1984; 158(3):1033-6. PMC: 215546. DOI: 10.1128/jb.158.3.1033-1036.1984. View

Riess T, Dietrich F, Schmidt K, Kaiser P, Schwarz H, Schafer A . Analysis of a novel insect cell culture medium-based growth medium for Bartonella species. Appl Environ Microbiol. 2008; 74(16):5224-7. PMC: 2519262. DOI: 10.1128/AEM.00621-08. View

Szczesny P, Linke D, Ursinus A, Bar K, Schwarz H, Riess T . Structure of the head of the Bartonella adhesin BadA. PLoS Pathog. 2008; 4(8):e1000119. PMC: 2483945. DOI: 10.1371/journal.ppat.1000119. View

Linke D, Riess T, Autenrieth I, Lupas A, Kempf V . Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 2006; 14(6):264-70. DOI: 10.1016/j.tim.2006.04.005. View

Cover T, Aber R . Yersinia enterocolitica. N Engl J Med. 1989; 321(1):16-24. DOI: 10.1056/NEJM198907063210104. View

Riess T, Andersson S, Lupas A, Schaller M, Schafer A, Kyme P . Bartonella adhesin a mediates a proangiogenic host cell response. J Exp Med. 2004; 200(10):1267-78. PMC: 2211922. DOI: 10.1084/jem.20040500. View

Roggenkamp A, Ruckdeschel K, Leitritz L, Schmitt R, Heesemann J . Deletion of amino acids 29 to 81 in adhesion protein YadA of Yersinia enterocolitica serotype O:8 results in selective abrogation of adherence to neutrophils. Infect Immun. 1996; 64(7):2506-14. PMC: 174104. DOI: 10.1128/iai.64.7.2506-2514.1996. View

10.

Leo J, Elovaara H, Bihan D, Pugh N, Kilpinen S, Raynal N . First analysis of a bacterial collagen-binding protein with collagen Toolkits: promiscuous binding of YadA to collagens may explain how YadA interferes with host processes. Infect Immun. 2010; 78(7):3226-36. PMC: 2897373. DOI: 10.1128/IAI.01057-09. View

11.

Eble J, Niland S . The extracellular matrix of blood vessels. Curr Pharm Des. 2009; 15(12):1385-400. DOI: 10.2174/138161209787846757. View

12.

Heise T, Dersch P . Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci U S A. 2006; 103(9):3375-80. PMC: 1413876. DOI: 10.1073/pnas.0507749103. View

13.

Hartmann H, Eltzschig H, Wurz H, Hantke K, Rakin A, Yazdi A . Hypoxia-independent activation of HIF-1 by enterobacteriaceae and their siderophores. Gastroenterology. 2008; 134(3):756-67. DOI: 10.1053/j.gastro.2007.12.008. View

14.

Schutz M, Weiss E, Schindler M, Hallstrom T, Zipfel P, Linke D . Trimer stability of YadA is critical for virulence of Yersinia enterocolitica. Infect Immun. 2010; 78(6):2677-90. PMC: 2876551. DOI: 10.1128/IAI.01350-09. View

15.

Roggenkamp A, Neuberger H, Flugel A, Schmoll T, Heesemann J . Substitution of two histidine residues in YadA protein of Yersinia enterocolitica abrogates collagen binding, cell adherence and mouse virulence. Mol Microbiol. 1995; 16(6):1207-19. DOI: 10.1111/j.1365-2958.1995.tb02343.x. View

16.

Tamm A, Tarkkanen A, Korhonen T, Kuusela P, TOIVANEN P, Skurnik M . Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica. Mol Microbiol. 1993; 10(5):995-1011. DOI: 10.1111/j.1365-2958.1993.tb00971.x. View

17.

Grosskinsky U, Schutz M, Fritz M, Schmid Y, Lamparter M, Szczesny P . A conserved glycine residue of trimeric autotransporter domains plays a key role in Yersinia adhesin A autotransport. J Bacteriol. 2007; 189(24):9011-9. PMC: 2168626. DOI: 10.1128/JB.00985-07. View

18.

Tertti R, Skurnik M, Vartio T, Kuusela P . Adhesion protein YadA of Yersinia species mediates binding of bacteria to fibronectin. Infect Immun. 1992; 60(7):3021-4. PMC: 257272. DOI: 10.1128/iai.60.7.3021-3024.1992. View

19.

Kaiser P, Riess T, Wagner C, Linke D, Lupas A, Schwarz H . The head of Bartonella adhesin A is crucial for host cell interaction of Bartonella henselae. Cell Microbiol. 2008; 10(11):2223-34. DOI: 10.1111/j.1462-5822.2008.01201.x. View

20.

Pries A, Secomb T, Gessner T, Sperandio M, Gross J, Gaehtgens P . Resistance to blood flow in microvessels in vivo. Circ Res. 1994; 75(5):904-15. DOI: 10.1161/01.res.75.5.904. View