Skip to main content

Advertisement

SpringerLink
Log in

Bacterial interactions with proteins and cells relevant to the development of life-threatening endocarditis studied by use of a quartz-crystal microbalance

  • Research Paper
  • Published:
Analytical and Bioanalytical Chemistry Aims and scope Submit manuscript

Abstract

Implant-related infections are a major challenge in clinical routine because of severe complications, for example infective endocarditis (IE). The purpose of this study was to investigate the real-time interaction of S. gordonii with proteins and cells important in the development of IE, in a flow system, by use of a quartz-crystal microbalance (QCM). Acoustic sensors were biologically modified by preconditioning with sterile saliva, platelet-poor plasma (PPP), or platelet-rich plasma (PRP), followed then by perfusion of a bacterial suspension. After perfusion, additional fluorescence and scanning electron microscopic (SEM) studies were performed. The surface structure of S. gordonii was analyzed by atomic force microscopy (AFM). Compared with S. gordonii adhesion on the abiotic sensor surface following normal mass loading indicated by a frequency decrease, adhesion on saliva, PPP, or PRP-conditioned sensors resulted in an increase in frequency. Furthermore, adhesion induced slightly increased damping signals for saliva and PPP-coated sensors but a decrease upon bacterial adhesion to PRP, indicating the formation of a more rigid biofilm. Microscopic analysis confirmed the formation of dense and vital bacterial layers and the aggregation of platelets and bacteria. In conclusion, our study shows that the complex patterns of QCM output data observed are strongly dependent on the biological substrate and adhesion mechanisms of S. gordonii. Overall, QCM sheds new light on the pathways of such severe infections as IE.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Tlaskalova-Hogenova H, Stepankova R, Hudcovic T, Tuckova L, Cukrowska B, Lodinova-Zadnikova R, Kozakova H, Rossmann P, Bartova J, Sokol D, Funda DP, Borovska D, Rehakova Z, Sinkora J, Hofman J, Drastich P, Kokesova A (2004) Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett 93(2–3):97–108

    Article  CAS  Google Scholar 

  2. Krismer B, Peschel A (2011) Does Staphylococcus aureus nasal colonization involve biofilm formation? Future Microbiol 6(5):489–493

    Article  Google Scholar 

  3. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108

    Article  CAS  Google Scholar 

  4. Jung CJ, Yeh CY, Shun CT, Hsu RB, Cheng HW, Lin CS, Chia JS (2012) Platelets enhance biofilm formation and resistance of endocarditis-inducing streptococci on the injured heart valve. J Infect Dis 205(7):1066–1075

    Article  CAS  Google Scholar 

  5. Moreillon P, Que YA (2004) Infective endocarditis. Lancet 363(9403):139–149

    Article  Google Scholar 

  6. Grainger DW, van der Mei HC, Jutted PC, van den Dungene JJAM, Schultz MJ, Van der Laang BFAM, Zaath SAJ, Busscher HJ (2013) Critical factors in the translation of improved antimicrobial strategies for medical implantsand devices. Biomaterials. doi:10.1016/j.biomaterials.2013.08.043

    Google Scholar 

  7. Kohavi D, Klinger A, Steinberg D, Sela MN (1995) Adsorption of salivary proteins onto prosthetic titanium components. J Prosthet Dent 74(5):531–534

    Article  CAS  Google Scholar 

  8. Eichler M, Katzur V, Scheideler L, Haupt M, Geis-Gerstorfer J, Schmalz G, Ruhl S, Muller R, Rupp F (2011) The impact of dendrimer-grafted modifications to model silicon surfaces on protein adsorption and bacterial adhesion. Biomaterials 32(35):9168–9179

    Article  CAS  Google Scholar 

  9. Rupp F, Haupt M, Eichler M, Doering C, Klostermann H, Scheideler L, Lachmann S, Oehr C, Wendel HP, Decker E, Geis-Gerstorfer J, von Ohle C (2012) Formation and photocatalytic decomposition of a pellicle on anatase surfaces. J Dent Res 91(1):104–109

    Article  CAS  Google Scholar 

  10. Schweikl H, Hiller K-A, Carl U, Schweiger R, Eidt A, Ruhl S, Müller R, Schmalz G (2013) Salivary protein adsorption and Streptococcus gordonii adhesion to dental material surfaces. Dent Mater. doi:10.1016/j.dental.2013.07.021

    Google Scholar 

  11. Fitzgerald JR, Foster TJ, Cox D (2006) The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 4(6):445–457

    Article  CAS  Google Scholar 

  12. Ivert TS, Dismukes WE, Cobbs CG, Blackstone EH, Kirklin JW, Bergdahl LA (1984) Prosthetic valve endocarditis. Circulation 69(2):223–232

    Article  CAS  Google Scholar 

  13. Kerrigan SW, Cox D (2010) Platelet-bacterial interactions. Cell Mol Life Sci 67(4):513–523

    Article  CAS  Google Scholar 

  14. Becker B, Cooper MA (2011) A survey of the 2006–2009 quartz-crystal microbalance biosensor literature. J Mol Recog: JMR 24(5):754–787. doi:10.1002/jmr.1117

    Article  CAS  Google Scholar 

  15. Guo X, Lin CS, Chen SH, Ye R, Wu VCH (2012) A piezoelectric immunosensor for specific capture and enrichment of viable pathogens by quartz-crystal microbalance sensor, followed by detection with antibody-functionalized gold nanoparticles. Biosens Bioelectron 38(1):177–183

    Article  CAS  Google Scholar 

  16. Su XL, Li YB (2004) A self-assembled monolayer-based piezoelectric immunosensor for rapid detection of Escherichia coli O157: H7. Biosens Bioelectron 19(6):563–574

    Article  CAS  Google Scholar 

  17. Knetsch MLW, Koole LH (2011) New Strategies in the Development of Antimicrobial Coatings: The Example of Increasing Usage of Silver and Silver Nanoparticles. Polym Basel 3(1):340–366. doi:10.3390/Polym3010340

    CAS  Google Scholar 

  18. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322

    Article  CAS  Google Scholar 

  19. Olsson ALJ, van der Mei HC, Busscher HJ, Sharma PK (2009) Influence of cell surface appendages on the bacterium-substratum interface measured real-time using QCM-D. Langmuir 25(3):1627–1632

    Article  CAS  Google Scholar 

  20. Rheinlaender J, Grabner A, Ott L, Burkovski A, Schaffer TE (2012) Contour and persistence length of Corynebacterium diphtheriae pili by atomic force microscopy. Eur Biophys J Biophys Lett 41(6):561–570

    Article  Google Scholar 

  21. Rodahl M, Hook F, Krozer A, Brzezinski P, Kasemo B (1995) Quartz-Crystal Microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments. Rev Sci Instrum 66(7):3924–3930

    Article  CAS  Google Scholar 

  22. Kanazawa KK, Gordon JG (1985) Frequency of a quartz microbalance in contact with liquid. Anal Chem 57(8):1770–1771

    Article  CAS  Google Scholar 

  23. Kanazawa KK, Gordon JG (1985) The oscillation frequency of a quartz resonator in contact with a liquid. Anal Chim Acta 175(SEP):99–105

    Article  CAS  Google Scholar 

  24. Sinn S, Muller L, Drechsel H, Wandel M, Northoff H, Ziemer G, Wendel HP, Gehring FK (2010) Platelet aggregation monitoring with a newly developed quartz-crystal microbalance system as an alternative to optical platelet aggregometry. Analyst 135(11):2930–2938

    Article  CAS  Google Scholar 

  25. Vanhoorelbeke K, Ulrichts H, Van de Walle G, Fontayne A, Deckmyn H (2007) Inhibition of platelet glycoprotein Ib and its Antithrombotic potential. Curr Pharm Des 13(26):2684–2697

    Article  CAS  Google Scholar 

  26. Marcus IM, Herzberg M, Walker SL, Freger V (2012) Pseudomonas aeruginosa attachment on QCM-D sensors: The role of cell and surface hydrophobicities. Langmuir 28(15):6396–6402

    Article  CAS  Google Scholar 

  27. Boks NP, Norde W, van der Mei HC, Busscher HJ (2008) Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. Microbiology 154(Pt 10):3122–3133. doi:10.1099/mic.0.2008/018622-0

    Article  CAS  Google Scholar 

  28. Bos R, van der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions—its mechanisms and methods for study. FEMS Microbiol Rev 23(2):179–230

    CAS  Google Scholar 

  29. Muller R, Eidt A, Hiller KA, Katzur V, Subat M, Schweikl H, Imazato S, Ruhl S, Schmalz G (2009) Influences of protein films on antibacterial or bacteria-repellent surface coatings in a model system using silicon wafers. Biomaterials 30(28):4921–4929. doi:10.1016/j.biomaterials.2009.05.079

    Article  Google Scholar 

  30. Puckett SD, Taylor E, Raimondo T, Webster TJ (2010) The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials 31(4):706–713. doi:10.1016/j.biomaterials.2009.09.081

    Article  CAS  Google Scholar 

  31. Gehring FK (2005) Schwingquarzsensorik in Flüssigkeiten: Entwicklung eines Blutanalysegerätes vol Auflage 1. Cuvillier, E.,

  32. Yombi JC, Belkhir L, Jonckheere S, Wilmes D, Cornu O, Vandercam B, Rodriguez-Villalobos H (2012) Streptococcus gordonii septic arthritis : two cases and review of literature. Bmc Infectious Diseases 12

  33. Sauerbrey G (1959) Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung. Z Phys A Hadrons Nucl 155(2):206–222. doi:10.1007/BF01337937

    CAS  Google Scholar 

  34. Voinova MV, Jonson M, Kasemo B (2002) Missing mass effect in biosensor's QCM applications. Biosens Bioelectron 17(10):835–841

    Article  CAS  Google Scholar 

  35. Hannig M (1997) Transmission electron microscopic study of in vivo pellicle formation on dental restorative materials. Eur J Oral Sci 105(5):422–433

    Article  CAS  Google Scholar 

  36. Olsson ALJ, van der Mei HC, Busscher HJ, Sharma PK (2011) Acoustic sensing of the bacterium-substratum interface using QCM-D and the influence of extracellular polymeric substances. J Colloid Interface Sci 357(1):135–138

    Article  CAS  Google Scholar 

  37. Dybwad GL (1985) A Sensitive New Method for the Determination of Adhesive Bonding between a Particle and a Substrate. J Appl Phys 58(7):2789–2790. doi:10.1063/1.335874

    Article  CAS  Google Scholar 

  38. McNab R, Forbes H, Handley PS, Loach DM, Tannock GW, Jenkinson HF (1999) Cell wall-anchored CshA polypeptide (259 kilodaltons) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties. J Bacteriol 181(10):3087–3095

    CAS  Google Scholar 

  39. Nobbs AH, Lamont RJ, Jenkinson HF (2009) Streptococcus adherence and colonization. Microbiology and molecular biology reviews. MMBR 73(3):407–450. doi:10.1128/MMBR.00014-09, Table of Contents

    Article  CAS  Google Scholar 

  40. Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS (2010) Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8(7):471–480. doi:10.1038/nrmicro2381

    Article  CAS  Google Scholar 

  41. Ruhl S, Sandberg AL, Cisar JO (2004) Salivary receptors for the proline-rich protein-binding and lectin-like adhesins of oral actinomyces and streptococci. J Dent Res 83(6):505–510

    Article  CAS  Google Scholar 

  42. Ahn SJ, Kho HS, Kim KK, Nahm DS (2003) Adhesion of oral streptococci to experimental bracket pellicles from glandular saliva. Am J Orthod Dentofac Orthop: Off Publ Am Assoc Orthod Constituent Soc Am Board Orthod 124(2):198–205. doi:10.1016/S0889540603003469

    Article  Google Scholar 

  43. Jenkinson HF, Lamont RJ (1997) Streptococcal adhesion and colonization. Crit Rev Oral Biol Med: Off Publ Am Assoc Oral Biologist 8(2):175–200

    Article  CAS  Google Scholar 

  44. Kerrigan SW, Jakubovics NS, Keane C, Maguire P, Wynne K, Jenkinson HF, Cox D (2007) Role of streptococcus gordonii surface proteins SspA/SspB and hsa in platelet function. Infect Immun 75(12):5740–5747

    Article  CAS  Google Scholar 

  45. Petersen HJ, Keane C, Jenkinson HF, Vickerman MM, Jesionowski A, Waterhouse JC, Cox D, Kerrigan SW (2010) Human platelets recognize a novel surface protein, PadA, on Streptococcus gordonii through a unique interaction involving fibrinogen receptor GPIIbIIIa. Infect Immun 78(1):413–422

    Article  CAS  Google Scholar 

Download references

Acknowledgement

The S. gordonii DL1 bacterial strain was kindly provided by Professor Stefan Ruhl (Buffalo, NY, USA). The technical assistance of I. Stephan (University Hospital Tübingen, Germany) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Thoracic, Cardiac and Vascular Surgery, Clinical Research Laboratory, University Hospital Tübingen, Calwerstr. 7/1, 72076, Tübingen, Germany

    Stefanie Krajewski, Denis Canjuga & Hans-Peter Wendel

  2. Institute of Applied Physics and LISA+, University of Tübingen, Auf der Morgenstelle 10, 72076, Tübingen, Germany

    Johannes Rheinlaender, Philip Ries & Tilman E. Schäffer

  3. Department of Prosthetic Dentistry, Section Medical Materials and Technology, University Hospital Tübingen, Osianderstr. 2-8, 72076, Tübingen, Germany

    Carmen Mack, Lutz Scheideler, Jürgen Geis-Gerstorfer & Frank Rupp

Authors
  1. Stefanie Krajewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johannes Rheinlaender
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philip Ries
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denis Canjuga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carmen Mack
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lutz Scheideler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tilman E. Schäffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jürgen Geis-Gerstorfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hans-Peter Wendel
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Frank Rupp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frank Rupp.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krajewski, S., Rheinlaender, J., Ries, P. et al. Bacterial interactions with proteins and cells relevant to the development of life-threatening endocarditis studied by use of a quartz-crystal microbalance. Anal Bioanal Chem 406, 3395–3406 (2014). https://doi.org/10.1007/s00216-014-7769-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00216-014-7769-9

Keywords

Search

Navigation