Zinc-dependent mechanical properties of Staphylococcus aureus biofilm-forming surface protein SasG

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 2, 2016, Pages 410-415

  Formosa Dague, Cécile ^a   Speziale, Pietro ^b   Foster, Timothy J ^c   Geoghegan, Joan A ^c   Dufrêne, Yves F ^a,d  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF PAVIA   (Italy)

^c TRINITY COLLEGE DUBLIN   (Ireland)

^d Walloon Excellence in Life Sciences and Biotechnology (WELBIO)   (Belgium)

Author keywords

Adhesion; Atomic force microscopy; Biofilms; SasG; Staphylococcus aureus

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; SURFACE PROTEIN SASG; UNCLASSIFIED DRUG; ZINC ION; SASG PROTEIN, STAPHYLOCOCCUS AUREUS; ZINC;

ADSORPTION; ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL CELL WALL; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; CELL ADHESION; CELL SURFACE; MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN UNFOLDING; SHEAR STRENGTH; SINGLE CELL ANALYSIS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS INFECTION; BIOLOGICAL MODEL; BIOMECHANICS; BIOPHYSICS; CELL MEMBRANE; CELL WALL; CHEMISTRY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; BIOMECHANICAL PHENOMENA; BIOPHYSICAL PHENOMENA; CELL MEMBRANE; CELL WALL; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; STAPHYLOCOCCUS AUREUS; ZINC;

EID: 84954513689     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1519265113     Document Type: Article

References (40)

1. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: A common cause of persistent infections. Science 284(5418):1318-1322.
2. López D, Vlamakis H, Kolter R (2010) Biofilms. Cold Spring Harb Perspect Biol 2(7): a000398.
3. Lister JL, Horswill AR (2014) Staphylococcus aureus biofilms: Recent developments in biofilm dispersal. Front Cell Infect Microbiol 4:178.
4. Hogan S, Stevens NT, Humphreys H, O'Gara JP, O'Neill E (2015) Current and future approaches to the prevention and treatment of staphylococcal medical device-related infections. Curr Pharm Des 21(1):100-113.
5. Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR (2015) Giving structure to the biofilm matrix: An overview of individual strategies and emerging common themes. FEMS Microbiol Rev 39(5):649-669.
6. Speziale P, Pietrocola G, Foster TJ, Geoghegan JA (2014) Protein-based biofilm matrices in Staphylococci. Front Cell Infect Microbiol 4:171.
7. Foster TJ, Geoghegan JA, Ganesh VK, Höök M (2014) Adhesion, invasion and evasion: The many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12(1):49-62.
8. Otto M (2008) Staphylococcal biofilms. Curr Top Microbiol Immunol 322:207-228.
9. Mack D, et al. (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: Purification and structural analysis. J Bacteriol 178(1):175-183.
10. O'Gara JP (2007) ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 270(2):179-188.
11. Laverty G, Gorman SP, Gilmore BF (2013) Biomolecular mechanisms of staphylococcal biofilm formation. Future Microbiol 8(4):509-524.
12. Corrigan RM, Rigby D, Handley P, Foster TJ (2007) The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 153(Pt 8): 2435-2446.
13. Geoghegan JA, et al. (2010) Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J Bacteriol 192(21):5663-5673.
14. Gruszka DT, et al. (2012) Staphylococcal biofilm-forming protein has a contiguous rod-like structure. Proc Natl Acad Sci USA 109(17):E1011-E1018.
15. Conrady DG, Wilson JJ, Herr AB (2013) Structural basis for Zn2+-dependent intercellular adhesion in staphylococcal biofilms. Proc Natl Acad Sci USA 110(3): E202-E211.
16. Decker R, et al. (2015) An 18 kDa scaffold protein is critical for Staphylococcus epidermidis biofilm formation. PLoS Pathog 11(3):e1004735.
17. Dufrêne YF (2014) Atomic force microscopy in microbiology: New structural and functional insights into the microbial cell surface. MBio 5(4):e01363-14.
18. Dufrêne YF (2015) Sticky microbes: Forces in microbial cell adhesion. Trends Microbiol 23(6):376-382.
19. Xu C-P, et al. (2008) Staphylococcus aureus-fibronectin interactions with and without fibronectin-binding proteins and their role in adhesion and desorption. Appl Environ Microbiol 74(24):7522-7528.
20. Francius G, Domenech O, Mingeot-Leclercq MP, Dufrêne YF (2008) Direct observation of Staphylococcus aureus cell wall digestion by lysostaphin. J Bacteriol 190(24): 7904-7909.
21. Lower SK, et al. (2010) A tactile response in Staphylococcus aureus. Biophys J 99(9): 2803-2811.
22. Casillas-Ituarte NN, Lower BH, Lamlertthon S, Fowler VG, Jr, Lower SK (2012) Dissociation rate constants of human fibronectin binding to fibronectin-binding proteins on living Staphylococcus aureus isolated from clinical patients. J Biol Chem 287(9): 6693-6701.
23. Heu C, Berquand A, Elie-Caille C, Nicod L (2012) Glyphosate-induced stiffening of Ha-CaT keratinocytes, a Peak Force Tapping study on living cells. J Struct Biol 178(1):1-7.
24. Alsteens D, et al. (2012) High-resolution imaging of chemical and biological sites on living cells using peak force tapping atomic force microscopy. Langmuir 28(49): 16738-16744.
25. Alsteens D, Trabelsi H, Soumillion P, Dufrêne YF (2013) Multiparametric atomic force microscopy imaging of single bacteriophages extruding from living bacteria. Nat Commun 4:2926.
26. Dufrêne YF, Martínez-Martín D, Medalsy I, Alsteens D, Müller DJ (2013) Multiparametric imaging of biological systems by force-distance curve-based AFM. Nat Methods 10(9):847-854.
27. Chopinet L, Formosa C, Rols MP, Duval RE, Dague E (2013) Imaging living cells surface and quantifying its properties at high resolution using AFM in QI™ mode. Micron 48: 26-33.
28. Formosa C, et al. (2015) Multiparametric imaging of adhesive nanodomains at the surface of Candida albicans by atomic force microscopy. Nanomedicine (Lond) 11(1): 57-65.
29. Helenius J, Heisenberg C-P, Gaub HE, Muller DJ (2008) Single-cell force spectroscopy. J Cell Sci 121(11):1785-1791.
30. Beaussart A, et al. (2013) Single-cell force spectroscopy of probiotic bacteria. Biophys J 104(9):1886-1892.
31. Touhami A, Nysten B, Dufrêne YF (2003) Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy. Langmuir 19(11):4539-4543.
32. Herman-Bausier P, El-Kirat-Chatel S, Foster TJ, Geoghegan JA, Dufrêne YF (2015) Staphylococcus aureus fibronectin-binding protein A mediates cell-cell adhesion through low-affinity homophilic bonds. MBio 6(3):e00413-e00415.
33. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276(5315):1109-1112.
34. Gruszka DT, et al. (2015) Cooperative folding of intrinsically disordered domains drives assembly of a strong elongated protein. Nat Commun 6:7271.
35. Conrady DG, et al. (2008) A zinc-dependent adhesion module is responsible for intercellular adhesion in staphylococcal biofilms. Proc Natl Acad Sci USA 105(49): 19456-19461.
36. Kellermayer MSZ, et al. (2005) Reversible mechanical unzipping of amyloid betafibrils. J Biol Chem 280(9):8464-8470.
37. Schaeffer CR, et al. (2015) Accumulation-associated protein enhances Staphylococcus epidermidis biofilm formation under dynamic conditions and is required for infection in a rat catheter model. Infect Immun 83(1):214-226.
38. Roche FM, Meehan M, Foster TJ (2003) The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149(Pt 10):2759-2767.
39. Köhler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256(5517):495-497.
40. Ebner A, et al. (2007) A new, simple method for linking of antibodies to atomic force microscopy tips. Bioconjug Chem 18(4):1176-1184.