Staphylococcus aureus Behavior on Artificial Surfaces Mimicking Bone Environment
Abstract
:1. Introduction
2. Materials and Methods
2.1. Coating Preparation
2.2. Bacterial Strains and Culture Media
2.3. Numeration of Viable Adherent Bacteria
2.4. Scanning Electron Microscopy (SEM)
2.5. Confocal Laser Scanning Microscopy (CLSM)
2.6. RT-qPCR (RNA Purification and Reverse Transcription)
2.7. Graphical Representation of Data and Statistical Analysis
3. Results
3.1. Bacterial Adhesion on Coated Supports Mimicking Bone Matrix
3.2. Initial Biofilm Structures and Composition on Collagen and CaP Supports
3.3. Initial Biofilm Formation-Related Gene Expression on Collagen and CaP Supports
3.4. Influence of the Simultaneous Presence of Different Coated Supports on S. aureus Adhesion
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Lu, J.; Yu, H.; Chen, C. Biological properties of calcium phosphate biomaterials for bone repair: A review. RSC Adv. 2018, 8, 2015–2033. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Y.; Liu, Y.; Li, R.; Bai, H.; Zhu, Z.; Zhu, L.; Zhu, C.; Che, Z.; Liu, H.; Wanf, J.; et al. Collagen-based biomaterials for bone tissue engineering. Mat. Design 2021, 210, 220049. [Google Scholar] [CrossRef]
- Kołodziejska, B.; Kaflak, A.; Kolmas, J. Biologically Inspired Collagen/Apatite Composite Biomaterials for Potential Use in Bone Tissue Regeneration—A Review. Materials 2020, 13, 1748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masters, E.A.; Trombetta, R.P.; de Mesy Bentley, K.L.; Boyce, B.F.; Gill, A.L.; Gill, S.R.; Nishitani, K.; Ishikawa, M.; Morita, Y.; Ito, H.; et al. Evolving concepts in bone infection: Redefining “biofilm”, “acute vs. chronic osteomyelitis”, “the immune proteome” and “local antibiotic therapy”. Bone Res. 2019, 7, 20. [Google Scholar] [CrossRef] [Green Version]
- Geurts, J.; Arts, J.; Walenkamp, G. Bone graft substitutes in active or suspected infection. Contra-indicated or not? Injury 2011, 42, S82–S86. [Google Scholar] [CrossRef] [Green Version]
- Lamret, F.; Colin, M.; Mongaret, C.; Gangloff, S.C.; Reffuveille, F. Antibiotic Tolerance of Staphylococcus aureus Biofilm in Periprosthetic Joint Infections and Antibiofilm Strategies. Antibiotics 2020, 9, 547. [Google Scholar] [CrossRef]
- Bjarnsholt, T.; Whiteley, M.; Rumbaugh, K.P.; Stewart, P.S.; Jensen, P.; Frimodt-Møller, N. The importance of understanding the infectious microenvironment. Lancet Infect. Dis. 2021, 22, e88–e92. [Google Scholar] [CrossRef]
- Antoine, E.E.; Vlachos, P.P.; Rylander, M.N. Review of collagen I hydrogels for bioengineered tissue microenvironments: Characterization of mechanics, structure, and transport. Tissue Eng. Part B Rev. 2014, 20, 683–696. [Google Scholar] [CrossRef] [Green Version]
- Strauss, K.; Chmielewski, J. Advances in the design and higher-order assembly of collagen mimetic peptides for regenerative medicine. Curr. Opin. Biotechnol. 2017, 46, 34–41. [Google Scholar] [CrossRef]
- Josse, J.; Velard, F.; Gangloff, S.C. Staphylococcus aureus vs. Osteoblast: Relationship and Consequences in Osteomyelitis. Front. Cell. Infect. Microbiol. 2015, 5, 85. [Google Scholar] [CrossRef] [Green Version]
- Mechiche Alami, S.; Rammal, H.; Boulagnon-Rombi, C.; Velard, F.; Lazar, F.; Drevet, R.; Laurent Maquin, D.; Gangloff, S.C.; Hemmerle, J.; Voegel, J.C.; et al. Harnessing Wharton’s jelly stem cell differentiation into bone-like nodule on calcium phosphate substrate without osteoinductive factors. Acta Biomater. 2017, 49, 575–589. [Google Scholar] [CrossRef] [Green Version]
- De la Fuente-Núñez, C.; Reffuveille, F.; Haney, E.F.; Straus, S.K.; Hancock, R.E.W. Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog. 2014, 10, e1004152. [Google Scholar] [CrossRef] [Green Version]
- Arciola, C.R.; Campoccia, D.; Ravaioli, S.; Montanaro, L. Polysaccharide intercellular adhesin in biofilm: Structural and regulatory aspects. Front. Cell. Infect. Microbiol. 2015, 5, 7. [Google Scholar] [CrossRef] [Green Version]
- Podlesek, Z.; Bertok, D.Ž. The DNA Damage Inducible SOS Response Is a Key Player in the Generation of Bacterial Persister Cells and Population Wide Tolerance. Front. Microbiol. 2020, 11, 1785. [Google Scholar] [CrossRef]
- Archer, N.K.; Mazaitis, M.J.; Costerton, J.W.; Leid, J.G.; Powers, M.E.; Shirtliff, M.E. Staphylococcus aureus biofilms: Properties, regulation, and roles in human disease. Virulence 2011, 2, 445–459. [Google Scholar] [CrossRef] [Green Version]
- Rice, K.C.; Mann, E.E.; Endres, J.L.; Weiss, E.C.; Cassat, J.E.; Smeltzer, M.S.; Bayles, K.W. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 2007, 104, 8113–8118. [Google Scholar] [CrossRef] [Green Version]
- Lauderdale, K.J.; Boles, B.R.; Cheung, A.L.; Horswill, A.R. Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect. Immun. 2009, 77, 1623–1635. [Google Scholar] [CrossRef] [Green Version]
- Tan, L.; Li, S.R.; Jiang, B.; Hu, X.M.; Li, S. Therapeutic Targeting of the Staphylococcus aureus Accessory Gene Regulator (agr) System. Front. Microbiol. 2018, 9, 55. [Google Scholar] [CrossRef]
- Foster, T.J.; Geoghegan, J.A.; Ganesh, V.K.; Höök, M. Adhesion, invasion and evasion: The many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 2014, 12, 49–62. [Google Scholar] [CrossRef] [Green Version]
- Arciola, C.R.; Campoccia, D.; Speziale, P.; Montanaro, L.; Costerton, J.W. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 2012, 33, 5967–5982. [Google Scholar] [CrossRef]
- Lamret, F.; Varin-Simon, J.; Velard, F.; Terryn, C.; Mongaret, C.; Colin, M.; Gangloff, S.C.; Reffuveille, F. Staphylococcus aureus Strain-Dependent Biofilm Formation in Bone-Like Environment. Front. Microbiol. 2021, 12, 2426. [Google Scholar] [CrossRef] [PubMed]
- Flemming, H.C.; Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 2010, 8, 623–633. [Google Scholar] [CrossRef] [PubMed]
- McCarthy, H.; Rudkin, J.; Black, N.; Egallagher, L.; O’Neill, E.; O’Gara, J.P. Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front. Cell. Infect. Microbiol. 2015, 5, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, T.; Flint, S.; Palmer, J. Magnesium and calcium ions: Roles in bacterial cell attachment and biofilm structure maturation. Biofouling 2019, 35, 959–974. [Google Scholar] [CrossRef]
- Domínguez, D.C.; Guragain, M.; Patrauchan, M. Calcium binding proteins and calcium signaling in prokaryotes. Cell Calcium 2015, 57, 151–165. [Google Scholar] [CrossRef]
- Schilcher, K.; Horswill, A.R. Staphylococcal Biofilm Development: Structure, Regulation, and Treatment Strategies. Microbiol. Mol. Biol. Rev. 2020, 84, e00026-19. [Google Scholar] [CrossRef]
- George, S.M.; Nayak, C.; Singh, I.; Balani, K. Multifunctional Hydroxyapatite Composites for Orthopedic Applications: A Review. ACS Biomater. Sci. Eng. 2022, 8, 3162–3186. [Google Scholar] [CrossRef]
- Dubus, M.; Varin-Simon, J.; Prada, P.; Scomazzon, L.; Reffuveille, F.; Alem, H.; Boulmedais, F.; Mauprivez, C.; Rammal, H.; Kerdjoudj, H. Biopolymers-calcium phosphate antibacterial coating reduces the pathogenicity of internalized bacteria by mesenchymal stromal cells. Biomater. Sci. 2020, 8, 5763–5773. [Google Scholar] [CrossRef]
Target Gene | Forward Primer | Reverse Primer |
---|---|---|
gyrB | CACGTGAAGGTATGACAGCA | ACAACTTGACGCACTTCAGA |
rho | AACGTGGGGATAAAGTAACTGG | TTCACTTCTTCTGCGTTATGGT |
recA | ATAGGTCGCCGAGTTTCAAC | GCGCTACTGTTGTCTTACCA |
lexA | TCAATATTTTCTACTGCGGTAATAGG | GAAACGATTCATGTGCCAGTT |
sigB | TTGTCCCATTTCCATTGCTT | CAGTGAAATAGCTGATCGATTAGAAG |
sarA | TTTCTCTTTGTTTTCGCTGATGT | TGTTATCAATGGTCACTTATGCTG |
agrB | ACAGTGAGGAGAGTGGTGTAA | AGCTAAGACCTGCATCCCTA |
rsh | CGAAACCTAATAACGTATCAAATGC | TGTATGTAGATCGAAAACCATCACT |
cidA | GATTGTACCGCTAACTTGGGT | GCGTAATTTCGGAAGCAACAT |
fnbpB | AATTAAATCAGAGCCGCCAGT | AATGGTACCTTCTGCATGACC |
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Lemaire, A.; Varin-Simon, J.; Lamret, F.; Dubus, M.; Kerdjoudj, H.; Velard, F.; Gangloff, S.C.; Reffuveille, F. Staphylococcus aureus Behavior on Artificial Surfaces Mimicking Bone Environment. Pathogens 2023, 12, 384. https://doi.org/10.3390/pathogens12030384
Lemaire A, Varin-Simon J, Lamret F, Dubus M, Kerdjoudj H, Velard F, Gangloff SC, Reffuveille F. Staphylococcus aureus Behavior on Artificial Surfaces Mimicking Bone Environment. Pathogens. 2023; 12(3):384. https://doi.org/10.3390/pathogens12030384
Chicago/Turabian StyleLemaire, Anaïs, Jennifer Varin-Simon, Fabien Lamret, Marie Dubus, Halima Kerdjoudj, Frédéric Velard, Sophie C. Gangloff, and Fany Reffuveille. 2023. "Staphylococcus aureus Behavior on Artificial Surfaces Mimicking Bone Environment" Pathogens 12, no. 3: 384. https://doi.org/10.3390/pathogens12030384
APA StyleLemaire, A., Varin-Simon, J., Lamret, F., Dubus, M., Kerdjoudj, H., Velard, F., Gangloff, S. C., & Reffuveille, F. (2023). Staphylococcus aureus Behavior on Artificial Surfaces Mimicking Bone Environment. Pathogens, 12(3), 384. https://doi.org/10.3390/pathogens12030384