Proteomic profile of the saliva and plasma protein layer adsorbed on Ti–Zr alloy: the effect of sandblasted and acid-etched surface treatment

References

• Abdallah MN, Abughanam G, Tran SD, Sheikh Z, Mezour MA, Basiri T, Xiao Y, Cerruti M, Siqueira WL, Tamimi F. 2018. Comparative adsorption profiles of basal lamina proteome and gingival cells onto dental and titanium surfaces. Acta Biomater. 73:547–558. doi:10.1016/j.actbio.2018.04.017
   PubMed Web of Science ®Google Scholar
• Al-Ahmad A, Wiedmann-Al-Ahmad M, Fackler A, Follo M, Hellwig E, Bächle M, Hannig C, Han J-S, Wolkewitz M, Kohal R, et al. 2013. In vivo study of the initial bacterial adhesion on different implant materials. Arch Oral Biol. 58:1139–1147. doi:10.1016/j.archoralbio.2013.04.011
   PubMed Web of Science ®Google Scholar
• Alayan J, Vaquette C, Saifzadeh S, Hutmacher D, Ivanovski S. 2017. Comparison of early osseointegration of SLA® and SLActive® implants in maxillary sinus augmentation: a pilot study. Clin Oral Impl Res. 28:1325–1333. doi:10.1111/clr.12988
   PubMed Web of Science ®Google Scholar
• Altuna P, Lucas-Taulé E, Gargallo-Albiol J, Figueras-Álvarez O, Hernández-Alfaro F, Nart J. 2016. Clinical evidence on titanium-zirconium dental implants: a systematic review and meta-analysis. Int J Oral Maxillofac Surg. 45:842–850. doi:10.1016/j.ijom.2016.01.004
   PubMed Web of Science ®Google Scholar
• Araújo-Gomes N, Romero-Gavilán F, Sánchez-Pérez AM, Gurruchaga M, Azkargorta M, Elortza F, Martinez-Ibañez M, Iloro I, Suay J, Goñi I, et al. 2018. Characterization of serum proteins attached to distinct sol-gel hybrid surfaces. J Biomed Mater Res Part B: Appl Biomater. 106:1477–1485. doi:10.1002/jbm.b.33954
   PubMed Web of Science ®Google Scholar
• Barão VAR, Ricomini-Filho AP, Faverani LP, Del Bel Cury AA, Sukotjo C, Monteiro DR, Yuan J-C, Mathew MT, do Amaral RC, Mesquita MF, et al. 2015. The role of nicotine, cotinine and caffeine on the electrochemical behavior and bacterial colonization to cp-Ti. Mater Sci Eng C. 56:114–124. doi:10.1016/j.msec.2015.06.026
   PubMed Web of Science ®Google Scholar
• Barter S, Stone P, Bragger U. 2012. A pilot study to evaluate the success and survival rate of titanium-zirconium implants in partially edentulous patients: results after 24 months of follow-Up. Clin Oral Implants Res. 23:873–881. doi:10.1111/j.1600-0501.2011.02231.x
   PubMed Web of Science ®Google Scholar
• Bollinger RR, Everett ML, Palestrant D, Love SD, Lin SS, Parker W. 2003. Human secretory immunoglobulin A may contribute to biofilm formation in the gut. Immunology. 109:580–587. doi:10.1046/j.1365-2567.2003.01700.x
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254. doi:10.1016/0003-2697(76)90527-3
   PubMed Web of Science ®Google Scholar
• Bragulla HH, Homberger DG. 2009. Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J Anat. 214:516–559. doi:10.1111/j.1469-7580.2009.01066.x
   PubMed Web of Science ®Google Scholar
• Bürgers R, Morsczeck C, Felthaus O, Gosau M, Beck HC, Reichert TE. 2018. Induced surface proteins of Staphylococcus [corrected] epidermidis adhering to titanium implant substrata. Clin Oral Investig. 22:2663–2668. doi:10.1007/s00784-018-2508-9
   PubMedGoogle Scholar
• Carlén A, Rüdiger SG, Loggner I, Olsson J. 2003. Bacteria-binding plasma proteins in pellicles formed on hydroxyapatite in vitro and on teeth in vivo. Oral Microbiol Immunol. 18:203–207. doi:10.1034/j.1399-302X.2003.00043.x
   PubMedGoogle Scholar
• Cavalcanti IMG, Ricomini Filho AP, Lucena-Ferreira SC, da Silva WJ, Paes Leme AF, Senna PM, Del Bel Cury AA. 2014. Salivary pellicle composition and multispecies biofilm developed on titanium nitrided by cold plasma. Arch Oral Biol. 59:695–703. doi:10.1016/j.archoralbio.2014.04.001
   PubMed Web of Science ®Google Scholar
• Cordeiro JM, Barão V. 2017. Is there scientific evidence favoring the substitution of commercially pure titanium with titanium alloys for the manufacture of dental implants? Mater Sci Eng C Mater Biol Appl. 71:1201–1215. doi:10.1016/j.msec.2016.10.025
   PubMed Web of Science ®Google Scholar
• Cordeiro JM, Faverani LP, Grandini CR, Rangel EC, Cruz NC, Nociti-Junior FH, Almeida AB, Vicente FB, Morais BRG, Barão VAR, et al. 2018. Characterization of chemically treated Ti–Zr system alloys for dental implant application. Mater Sci Eng C Mater Biol Appl. 92:849–861. doi:10.1016/j.msec.2018.07.046
   PubMed Web of Science ®Google Scholar
• Diaz PI, Chalmers NI, Rickard AH, Kong C, Milburn CL, Palmer RJ, Jr, Kolenbrander PE. 2006. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl Environ Microbiol. 72:2837–2848. doi:10.1128/AEM.72.4.2837-2848.2006
   PubMed Web of Science ®Google Scholar
• Dini C, Costa RC, Sukotjo C, Takoudis CG, Mathew MT, Barão V. 2020. Progression of bio-tribocorrosion in implant dentistry. Front Mech Eng. 6:1. doi:10.3389/fmech.2020.00001
   Web of Science ®Google Scholar
• Dodo CG, Senna PM, Custodio W, Paes Leme AF, Del Bel Cury AA. 2013. Proteome analysis of the plasma protein layer adsorbed to a rough titanium surface. Biofouling. 29:549–557. doi:10.1080/08927014.2013.787416
   PubMed Web of Science ®Google Scholar
• Esberg A, Isehed C, Holmlund A, Lundberg P. 2019. Peri-implant crevicular fluid proteome before and after adjunctive enamel matrix derivative treatment of peri-implantitis. J. Clin. Periodontol. 46:669–677. doi:10.1111/jcpe.13108
   PubMed Web of Science ®Google Scholar
• Grandin HM, Berner S, Dard M. 2012. A review of titanium zirconium (TiZr) alloys for use in endosseous dental implants. Materials. 5:1348–1360. doi:10.3390/ma5081348
   Web of Science ®Google Scholar
• Grassl N, Kulak NA, Pichler G, Geyer PE, Jung J, Schubert S, Sinitcyn P, Cox J, Mann M. 2016. Ultra-deep and quantitative saliva proteome reveals dynamics of the oral microbiome. Genome Med. 8:44 doi:10.1186/s13073-016-0293-0
   PubMed Web of Science ®Google Scholar
• Guha Thakurta S, Subramanian A. 2011. Evaluation of in situ albumin binding surfaces: a study of protein adsorption and platelet adhesion. J Mater Sci Mater Med. 22:137–149. doi:10.1007/s10856-010-4169-3
   PubMed Web of Science ®Google Scholar
• Heberle H, Meirelles VG, da Silva FR, Telles GP, Minghim R. 2015. InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics. 16:1–7.
   PubMed Web of Science ®Google Scholar
• Hotchkiss KM, Reddy GB, Hyzy SL, Schwartz Z, Boyan BD, Olivares-Navarrete R. 2016. Titanium surface characteristics, including topography and wettability, alter macrophage activation. Acta Biomater. 31:425–434. doi:10.1016/j.actbio.2015.12.003
   PubMed Web of Science ®Google Scholar
• Hu S, Loo JA, Wong DT. 2007. Human saliva proteome analysis and disease biomarker discovery. Expert Rev Proteomics. 4:531–538. doi:10.1586/14789450.4.4.531
   PubMed Web of Science ®Google Scholar
• Hu XL, Ho B, Lim CT, Hsu CS. 2011. Thermal treatments modulate bacterial adhesion to dental enamel. J Dent Res. 90:1451–1456. doi:10.1177/0022034511424155
   PubMed Web of Science ®Google Scholar
• Jemat A, Ghazali MJ, Razali M, Otsuka Y. 2015. Surface modifications and their effects on titanium dental implants. Biomed Res Int. 2015:791725
   PubMed Web of Science ®Google Scholar
• Kalasin S, Santore MM. 2009. Non-specific adhesion on biomaterial surfaces driven by small amounts of protein adsorption. Colloids Surf B Biointerfaces. 73:229–236. doi:10.1016/j.colsurfb.2009.05.028
   PubMed Web of Science ®Google Scholar
• Kawahara R, Lima RN, Domingues RR, Pauletti BA, Meirelles GV, Assis M, Figueira ACM, Leme A. 2014. Deciphering the role of the ADAM17-dependent secretome in cell signaling. J Proteome Res. 13:2080–2093. doi:10.1021/pr401224u
   PubMed Web of Science ®Google Scholar
• Kim J. 2020. Systematic approach to characterize the dynamics of protein adsorption on the surface of biomaterials using proteomics. Colloids Surf B Biointerfaces. 188:110756 doi:10.1016/j.colsurfb.2019.110756
   PubMed Web of Science ®Google Scholar
• Kinnari TJ, Peltonen LI, Kuusela P, Kivilahti J, Könönen M, Jero J. 2005. Bacterial adherence to titanium surface coated with human serum albumin. Otol. Neurotol. 26:380–384. doi:10.1097/01.mao.0000169767.85549.87
   PubMed Web of Science ®Google Scholar
• Kronström M, Svensson B, Erickson E, Houston L, Braham P, Persson GR. 2000. Humoral immunity host factors in subjects with failing or successful titanium dental implants. J Clin Periodontol. 27:875–882. doi:10.1034/j.1600-051x.2000.027012875.x
   PubMed Web of Science ®Google Scholar
• Lee YH, Zimmerman JN, Custodio W, Xiao Y, Basiri T, Hatibovic-Kofman S, Siqueira WL. 2013. Proteomic evaluation of acquired enamel pellicle during in vivo formation. PLoS One. 8:e67919 doi:10.1371/journal.pone.0067919
   PubMed Web of Science ®Google Scholar
• Lendenmann U, Grogan J, Oppenheim FG. 2000. Saliva and dental pellicle-a review. Adv Dent Res. 14:22–28. doi:10.1177/08959374000140010301
   PubMedGoogle Scholar
• Lima EM, Koo H, Vacca Smith AM, Rosalen PL, Del Bel Cury AA. 2008. Adsorption of salivary and serum proteins, and bacterial adherence on titanium and zirconia ceramic surfaces. Clin Oral Implants Res. 19:780–785. doi:10.1111/j.1600-0501.2008.01524.x
   PubMed Web of Science ®Google Scholar
• Loo JA, Yan W, Ramachandran P, Wong DT. 2010. Comparative human salivary and plasma proteomes. J Dent Res. 89:1016–1023. doi:10.1177/0022034510380414
   PubMed Web of Science ®Google Scholar
• Lori JA, Nok AJ. 2004. Mechanism of adsorption of mucin to titanium in vitro. Biomed Mater Eng. 14:557–563.
   PubMed Web of Science ®Google Scholar
• Lü X, Zhang H, Huang Y, Zhang Y. 2018. A proteomics study to explore the role of adsorbed serum proteins for PC12 cell adhesion and growth on chitosan and collagen/chitosan surfaces. Regen Biomater. 5:261–273. doi:10.1093/rb/rby017
   PubMed Web of Science ®Google Scholar
• Marković A, Đinić A, Calvo Guirado JL, Tahmaseb A, Šćepanović M, Janjić B. 2017. Randomized clinical study of the peri-implant healing to hydrophilic and hydrophobic implant surfaces in patients receiving anticoagulants. Clin Oral Implants Res. 28:1241–1247. doi:10.1111/clr.12948
   PubMed Web of Science ®Google Scholar
• Marsh PD, Moter A, Devine DA. 2011. Dental plaque biofilms: communities, conflict and control. Periodontol 2000. 55:16–35. doi:10.1111/j.1600-0757.2009.00339.x
   PubMed Web of Science ®Google Scholar
• Mukai Y, Torii M, Urushibara Y, Kawai T, Takahashi Y, Nobuko M, Ohkubo C, Ohshima T. 2020. Analysis of plaque microbiota and salivary proteins adhering to dental materials. J Oral Biosci. doi: 10.1016/j.job.2020.02.003
   PubMedGoogle Scholar
• Murphy M, Walczak MS, Thomas AG, Silikas N, Berner S, Lindsay R. 2017. Toward optimizing dental implant performance: surface characterization of Ti and TiZr implant materials. Denta Mater. 33:43–53. d doi:10.1016/j.dental.2016.10.001
   PubMed Web of Science ®Google Scholar
• Nicolau P, Guerra F, Reis R, Krafft T, Benz K, Jackowski J. 2019. 10-year outcomes with immediate and early loaded implants with a chemically modified SLA surface. Quintessence Int. 50:114–124.
   PubMed Web of Science ®Google Scholar
• Nygren H. 1996. Initial reactions of whole blood with hydrophilic and hydrophobic titanium surfaces. Colloids Surf B Biointerfaces. 6:329–333. doi:10.1016/0927-7765(96)01270-2
   Web of Science ®Google Scholar
• Othman Z, Cillero Pastor B, van Rijt S, Habibovic P. 2018. Understanding interactions between biomaterials and biological systems using proteomics. Biomaterials. 167:191–204. doi:10.1016/j.biomaterials.2018.03.020
   PubMed Web of Science ®Google Scholar
• Pantaroto HN, Amorim KP, Matozinho Cordeiro J, Souza JGS, Ricomini-Filho AP, Rangel EC, Ribeiro ALR, Vaz LG, Barão V. 2019. Proteome analysis of the salivary pellicle formed on titanium alloys containing niobium and zirconium. Biofouling. 35:173–186. doi:10.1080/08927014.2019.1580360
   PubMed Web of Science ®Google Scholar
• Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, Sahasrabudhe A, Dewhirst FE. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183:3770–3783. doi:10.1128/JB.183.12.3770-3783.2001
   PubMed Web of Science ®Google Scholar
• Rabe M, Verdes D, Seeger S. 2011. Understanding protein adsorption phenomena at solid surfaces. Adv Colloid Interface Sci. 162:87–106. doi:10.1016/j.cis.2010.12.007
   PubMed Web of Science ®Google Scholar
• Roehling S, Astasov-Frauenhoffer M, Hauser-Gerspach I, Braissant O, Woelfler H, Waltimo T, Kniha H, Gahlert M. 2017. In vitro biofilm formation on titanium and zirconia implant surfaces. J. Periodontol. 88:298–307. doi:10.1902/jop.2016.160245
   PubMed Web of Science ®Google Scholar
• Romero-Gavilán F, Gomes NC, Ródenas J, Sánchez A, Azkargorta M, Iloro I, Elortza F, García Arnáez I, Gurruchaga M, Goñi I, et al. 2017. Proteome analysis of human serum proteins adsorbed onto different titanium surfaces used in dental implants. Biofouling. 33:98–111. doi:10.1080/08927014.2016.1259414
   PubMed Web of Science ®Google Scholar
• Sela MN, Badihi L, Rosen G, Steinberg D, Kohavi D. 2007. Adsorption of human plasma proteins to modified titanium surfaces. Clin Oral Implants Res. 18:630–638. doi:10.1111/j.1600-0501.2007.01373.x
   PubMed Web of Science ®Google Scholar
• Siqueira WL, Custodio W, McDonald EE. 2012. New insights into the composition and functions of the acquired enamel pellicle. J Dent Res. 91:1110–1118. doi:10.1177/0022034512462578
   PubMed Web of Science ®Google Scholar
• Souza JGS, Bertolini M, Costa RC, Cordeiro JM, Nagay BE, de Almeida AB, Retamal-Valdes B, Nociti FH, Feres M, Rangel EC, et al. 2020. Targeting pathogenic bbiofilms: newly ddeveloped superhydrophobic coating favors a host-compatible microbial profile on the titanium surface. ACS Appl Mater Interfaces. 12:10118–10129. doi:10.1021/acsami.9b22741
   PubMed Web of Science ®Google Scholar
• Souza JGS, Bertolini M, Thompson A, Mansfield JM, Grassmann AA, Maas K, Caimano MJ, Barao VAR, Vickerman MM, Dongari-Bagtzoglou A, et al. 2020b. Role of glucosyltransferase R in biofilm interactions between Streptococcus oralis and Candida albicans. ISME J. 14:1207–1222. doi:10.1038/s41396-020-0608-4
   PubMed Web of Science ®Google Scholar
• Souza JGS, Lima CV, Costa Oliveira BE, Ricomini-Filho AP, Faveri M, Sukotjo C, Feres M, Del Bel Cury AA, Barão V. 2018. Dose-response effect of chlorhexidine on a multispecies oral biofilm formed on pure titanium and on a titanium-zirconium alloy. Biofouling. 34:1175–1184. doi:10.1080/08927014.2018.1557151
   PubMed Web of Science ®Google Scholar
• Taborelli M, Jobin M, François P, Vaudaux P, Tonetti M, Szmukler-Moncler S, Simpson JP, Descouts P. 1997. Influence of surface treatments developed for oral implants on the physical and biological properties of titanium. (I) Surface characterization. Clin Oral Implants Res. 8:208–216. doi:10.1034/j.1600-0501.1997.080307.x
   PubMed Web of Science ®Google Scholar
• Terheyden H, Lang NP, Bierbaum S, Stadlinger B. 2012. Osseointegration-communication of cells. Clin Oral Implants Res. 23:1127–1135. doi:10.1111/j.1600-0501.2011.02327.x
   PubMed Web of Science ®Google Scholar
• Van Velzen FJ, Ofec R, Schulten EA, Ten Bruggenkate CM. 2015. 10-year survival rate and the incidence of peri-implant disease of 374 titanium dental implants with a SLA surface: a prospective cohort study in 177 fully and partially edentulous patients. Clin Oral Implants Res. 26:1121–1128. doi:10.1111/clr.12499
   PubMed Web of Science ®Google Scholar
• Wennerberg A, Svanborg LM, Berner S, Andersson M. 2013. Spontaneously formed nanostructures on titanium surfaces. Clin Oral Implants Res. 24:203–209. doi:10.1111/j.1600-0501.2012.02429.x
   PubMed Web of Science ®Google Scholar
• Whittaker CJ, Klier CM, Kolenbrander PE. 1996. Mechanisms of adhesion by oral bacteria. Annu Rev Microbiol. 50:513–552. doi:10.1146/annurev.micro.50.1.513
   PubMed Web of Science ®Google Scholar
• Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. 2005. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng. 11:1–18. doi:10.1089/ten.2005.11.1
   PubMedGoogle Scholar
• Wittmer CR, Phelps JA, Saltzman WM, Van Tassel PR. 2007. Fibronectin terminated multilayer films: protein adsorption and cell attachment studies. Biomaterials. 28:851–860. doi:10.1016/j.biomaterials.2006.09.037
   PubMed Web of Science ®Google Scholar
• Xu LC, Bauer JW, Siedlecki CA. 2014. Proteins, platelets, and blood coagulation at biomaterial interfaces. Colloids Surf B Biointerfaces. 124:49–68. doi:10.1016/j.colsurfb.2014.09.040
   PubMed Web of Science ®Google Scholar
• Yan W, Apweiler R, Balgley BM, Boontheung P, Bundy JL, Cargile BJ, Cole S, Fang X, Gonzalez-Begne M, Griffin TJ, et al. 2009. Systematic comparison of the human saliva and plasma proteomes. Proteomics Clin Appl. 3:116–134. doi:10.1002/prca.200800140
   PubMed Web of Science ®Google Scholar
• Yang D, Lü X, Hong Y, Xi T, Zhang D. 2013. The molecular mechanism of mediation of adsorbed serum proteins to endothelial cells adhesion and growth on biomaterials. Biomaterials. 34:5747–5758. doi:10.1016/j.biomaterials.2013.04.028
   PubMed Web of Science ®Google Scholar
• Yeo IL. 2019. Modifications of dental implant surfaces at the micro- and nano-level for enhanced osseointegration. Materials (Basel.). 13:89 pii: doi:10.3390/ma13010089
   Web of Science ®Google Scholar
• Yin L, Chang Y, You Y, Liu C, Li J, Lai HC. 2019. Biological responses of human bone mesenchymal stem cells to Ti and TiZr implant materials. Clin Implant Dent Relat Res. 21:550–564.
   PubMed Web of Science ®Google Scholar