Roughness affects the response of human fibroblasts and macrophages to sandblasted abutments.
Peri-implant attachment
Protein adsorption
Proteomics
Soft-tissue healing
Titanium implants
Journal
Biomedical engineering online
ISSN: 1475-925X
Titre abrégé: Biomed Eng Online
Pays: England
ID NLM: 101147518
Informations de publication
Date de publication:
17 Jul 2024
17 Jul 2024
Historique:
received:
15
03
2024
accepted:
03
07
2024
medline:
18
7
2024
pubmed:
18
7
2024
entrez:
17
7
2024
Statut:
epublish
Résumé
A strong seal of soft-tissue around dental implants is essential to block pathogens from entering the peri-implant interface and prevent infections. Therefore, the integration of soft-tissue poses a challenge in implant-prosthetic procedures, prompting a focus on the interface between peri-implant soft-tissues and the transmucosal component. The aim of this study was to analyse the effects of sandblasted roughness levels on in vitro soft-tissue healing around dental implant abutments. In parallel, proteomic techniques were applied to study the interaction of these surfaces with human serum proteins to evaluate their potential to promote soft-tissue regeneration. Grade-5 machined titanium discs (MC) underwent sandblasting with alumina particles of two sizes (4 and 8 μm), resulting in two different surface types: MC04 and MC08. Surface morphology and roughness were characterised employing scanning electron microscopy and optical profilometry. Cell adhesion and collagen synthesis, as well as immune responses, were assessed using human gingival fibroblasts (hGF) and macrophages (THP-1), respectively. The profiles of protein adsorption to the surfaces were characterised using proteomics; samples were incubated with human serum, and the adsorbed proteins analysed employing nLC-MS/MS. hGFs exposed to MC04 showed decreased cell area compared to MC, while no differences were found for MC08. hGF collagen synthesis increased after 7 days for MC08. THP-1 macrophages cultured on MC04 and MC08 showed a reduced TNF-α and increased IL-4 secretion. Thus, the sandblasted topography led a reduction in the immune/inflammatory response. One hundred seventy-six distinct proteins adsorbed on the surfaces were identified. Differentially adsorbed proteins were associated with immune response, blood coagulation, angiogenesis, fibrinolysis and tissue regeneration. Increased roughness through MC08 treatment resulted in increased collagen synthesis in hGF and resulted in a reduction in the surface immune response in human macrophages. These results correlate with the changes in protein adsorption on the surfaces observed through proteomics.
Sections du résumé
BACKGROUND
BACKGROUND
A strong seal of soft-tissue around dental implants is essential to block pathogens from entering the peri-implant interface and prevent infections. Therefore, the integration of soft-tissue poses a challenge in implant-prosthetic procedures, prompting a focus on the interface between peri-implant soft-tissues and the transmucosal component. The aim of this study was to analyse the effects of sandblasted roughness levels on in vitro soft-tissue healing around dental implant abutments. In parallel, proteomic techniques were applied to study the interaction of these surfaces with human serum proteins to evaluate their potential to promote soft-tissue regeneration.
RESULTS
RESULTS
Grade-5 machined titanium discs (MC) underwent sandblasting with alumina particles of two sizes (4 and 8 μm), resulting in two different surface types: MC04 and MC08. Surface morphology and roughness were characterised employing scanning electron microscopy and optical profilometry. Cell adhesion and collagen synthesis, as well as immune responses, were assessed using human gingival fibroblasts (hGF) and macrophages (THP-1), respectively. The profiles of protein adsorption to the surfaces were characterised using proteomics; samples were incubated with human serum, and the adsorbed proteins analysed employing nLC-MS/MS. hGFs exposed to MC04 showed decreased cell area compared to MC, while no differences were found for MC08. hGF collagen synthesis increased after 7 days for MC08. THP-1 macrophages cultured on MC04 and MC08 showed a reduced TNF-α and increased IL-4 secretion. Thus, the sandblasted topography led a reduction in the immune/inflammatory response. One hundred seventy-six distinct proteins adsorbed on the surfaces were identified. Differentially adsorbed proteins were associated with immune response, blood coagulation, angiogenesis, fibrinolysis and tissue regeneration.
CONCLUSIONS
CONCLUSIONS
Increased roughness through MC08 treatment resulted in increased collagen synthesis in hGF and resulted in a reduction in the surface immune response in human macrophages. These results correlate with the changes in protein adsorption on the surfaces observed through proteomics.
Identifiants
pubmed: 39020369
doi: 10.1186/s12938-024-01264-6
pii: 10.1186/s12938-024-01264-6
doi:
Substances chimiques
Titanium
D1JT611TNE
Collagen
9007-34-5
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
68Subventions
Organisme : European Union-NextGenerationEU
ID : MGS/2022/10 (UP2022-024)
Organisme : Ministerio Ciencia e Innovación
ID : PDC2021-120924-I00/ AEI/10.13039/501100011033/ Unión Europea NextGenerationEU/PRTR
Organisme : Universitat Jaume I
ID : UJI-B2021-25
Informations de copyright
© 2024. The Author(s).
Références
Jordana F, Susbielles L, Colat-Parros J. Periimplantitis and implant body roughness: a systematic review of literature. Implant Dent. 2018;27:672–81.
Rinke S, Ohl S, Ziebolz D, Lange K, Eickholz P. Prevalence of periimplant disease in partially edentulous patients: a practice-based cross-sectional study. Clin Oral Implants Res. 2011;22:826–33.
Chen Z, Wang Z, Qiu W, Fang F. Overview of antibacterial strategies of dental implant materials for the prevention of peri-implantitis. Bioconjug Chem. 2021;32:627–38.
Guo T, Gulati K, Arora H, Han P, Fournier B, Ivanovski S. Orchestrating soft tissue integration at the transmucosal region of titanium implants. Acta Biomater. 2021;124:33–49. https://doi.org/10.1016/j.actbio.2021.01.001 .
Atsuta I, Ayukawa Y, Kondo R, Oshiro W, Matsuura Y, Furuhashi A, et al. Soft tissue sealing around dental implants based on histological interpretation. J Prosthodont Res. 2016;60:3–11. https://doi.org/10.1016/j.jpor.2015.07.001 .
Guo T, Gulati K, Arora H, Han P, Fournier B, Ivanovski S. Race to invade: understanding soft tissue integration at the transmucosal region of titanium dental implants. Dent Mater. 2021;37:816–31.
Mustafa K, Odén A, Wennerberg A, Hultenby K, Arvidson K. The influence of surface topography of ceramic abutments on the attachment and proliferation of human oral fibroblasts. Biomaterials. 2005;26:373–81.
Guillem-Marti J, Delgado L, Godoy-Gallardo M, Pegueroles M, Herrero M, Gil FJ. Fibroblast adhesion and activation onto micro-machined titanium surfaces. Clin Oral Implants Res. 2013;24:770–80.
Osman MA, Alamoush RA, Kushnerev E, Seymour KG, Watts DC, Yates JM. Biological response of epithelial and connective tissue cells to titanium surfaces with different ranges of roughness: an in-vitro study. Dent Mater. 2022;38:1777–88. https://doi.org/10.1016/j.dental.2022.09.010 .
Jie C, Wang T, Yinfei P, Zhihui T, Huanxin M. Influence on proliferation and adhesion of human gingival fibroblasts from different titanium surface decontamination treatments: an in vitro study. Arch Oral Biol. 2018;87:204–10.
Lyu Z, Yu Q, Chen H. Interactions of biomaterials surfaces with proteins and cells. In: Gao C, editor. Polym biomater tissue regen from surface/interface des to 3D Constr. Singapore: Springer; 2016. p. 103–22. https://doi.org/10.1007/978-981-10-2293-7
Romero-Gavilán F, Gomes NC, Ródenas J, Sánchez A, Mikel A, IbonIloro F, Elortza IGA, et al. Proteome analysis of human serum proteins adsorbed onto different titanium surfaces used in dental implants. Biofouling. 2017;33:98–111.
Romero-Gavilán F, Sanchez-Pérez AM, Araújo-Gomes N, Azkargorta M, Iloro I, Elortza F, et al. Proteomic analysis of silica hybrid sol-gel coatings: a potential tool for predicting the biocompatibility of implants in vivo. Biofouling. 2017;33:676–89.
Calciolari E, Donos N. The use of omics profiling to improve outcomes of bone regeneration and osseointegration How far are we from personalized medicine in dentistry? J Proteomics. 2018;18:30048–54.
García-Arnáez I, Romero-Gavilán F, Cerqueira A, Elortza F, Azkargorta M, Muñoz F, et al. Correlation between biological responses in vitro and in vivo to Ca-doped sol-gel coatings assessed using proteomic analysis. Colloids Surfaces B Biointerfaces. 2022;220:112962.
Cerqueira A, Romero-Gavilán F, García-Arnáez I, Martinez-Ramos C, Ozturan S, Izquierdo R, et al. Characterization of magnesium doped sol-gel biomaterial for bone tissue regeneration: the effect of Mg ion in protein adsorption. Mater Sci Eng C. 2021;125: 112114.
Romero-Gavilán F, Cerqueira A, García-Arnáez I, Azkargorta M, Elortza F, Gurruchaga M, et al. Proteomic evaluation of human osteoblast responses to titanium implants over time. J Biomed Mater Res Part A. 2023;111:45–59.
Matos GRM. Surface roughness of dental implant and osseointegration. J Maxillofac Oral Surg. 2021;20:1–4. https://doi.org/10.1007/s12663-020-01437-5 .
Shirazi S, Ravindran S, Cooper LF. Topography-mediated immunomodulation in osseointegration. Ally Enemy Biomater. 2022;291: 121903. https://doi.org/10.1016/j.biomaterials.2022.121903 .
Barberi J, Spriano S. Titanium and protein adsorption: an overview of mechanisms and effects of surface features. Materials (Basel). 2021;14:1590.
Araújo-Gomes N, Romero-Gavilán F, Sánchez-Pérez AM, Gurruchaga M, Azkargorta M, Elortza F, et al. Characterization of serum proteins attached to distinct sol–gel hybrid surfaces. J Biomed Mater Res Part B Appl Biomater. 2018;106:1477–85.
Akiyama Y, Iwasa F, Hotta Y, Matsumoto T, Oshima Y, Baba K. Effects of surface roughness of ceria-stabilized zirconia/alumina nanocomposite on the morphology and function of human gingival fibroblasts. Dent Mater J. 2021;40:472–80.
Yanagisawa N, Ikeda T, Takatsu M, Urata K, Nishio K, Tanaka H, et al. Human gingival fibroblast attachment to smooth titanium disks with different surface roughnesses. Biomimetics. 2022;7:164.
Rausch MA, Shokoohi-tabrizi H, Wehner C, Pippenger BE, Wagner RS, Ulm C, et al. Impact of implant surface material and microscale roughness on the initial attachment and proliferation of primary human gingival fibroblasts. Biology (Basel). 2021;10:356.
Wieland M, Chehroudi B, Textor M, Brunette DM. Use of Ti-coated replicas to investigate the effects on fibroblast shape of surfaces with varying roughness and constant chemical composition. J Biomed Mater Res. 2002;60:434–44.
Laleman I, Lambert F. Implant connection and abutment selection as a predisposing and/or precipitating factor for peri-implant diseases: a review. Clin Implant Dent Relat Res. 2023;25:723–33.
Rodriguez-González R, Monsalve-Guil L, Jimenez-Guerra A, Velasco-Ortega E, Moreno-Muñoz J, Nuñez-Marquez E, et al. Relevant aspects of titanium topography for osteoblastic adhesion and inhibition of bacterial colonization. Materials (Basel). 2023;16:1–13.
Petrini M, Giuliani A, Di Campli E, Di Lodovico S, Iezzi G, Piattelli A, et al. The bacterial anti-adhesive activity of double-etched titanium (Dae) as a dental implant surface. Int J Mol Sci. 2020;21:1–16.
Xing R, Lyngstadaas SP, Ellingsen JE, Taxt-Lamolle S, Haugen HJ. The influence of surface nanoroughness, texture and chemistry of TiZr implant abutment on oral biofilm accumulation. Clin Oral Implants Res. 2015;26:649–56.
Mamilos A, Winter L, Schmitt VH, Barsch F, Grevenstein D, Wagner W, et al. Macrophages: from simple phagocyte to an integrative regulatory cell for inflammation and tissue regeneration—a review of the literature. Cells. 2023;12:276.
Spiller KL, Nassiri S, Witherel CE, Anfang RR, Ng J, Nakazawa KR, et al. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds. Biomaterials. 2015;37:194–207.
Wang X, Wang Y, Bosshardt DD, Miron RJ, Zhang Y. The role of macrophage polarization on fibroblast behavior-an in vitro investigation on titanium surfaces. Clin Oral Investig. 2018;22:847–57.
Wu J, Yu P, Lv H, Yang S, Wu Z. Nanostructured zirconia surfaces regulate human gingival fibroblasts behavior through differential modulation of macrophage polarization. Front Bioeng Biotechnol. 2021;8:1–14.
Miao X, Wang D, Xu L. The response of human osteoblasts, epithelial cells, fibroblasts, macrophages and oral bacteria to nanostructured titanium surfaces: a systematic study (Int J Nanomedicine, (2017) 12, (1415–1430), https://doi.org/10.2147/IJN.S126760 ). Int J Nanomed. 2020;15:2351–2.
Lackington WA, Fleyshman L, Schweizer P, Elbs-Glatz Y, Guimond S, Rottmar M. The response of soft tissue cells to Ti implants is modulated by blood-implant interactions. Mater Today Bio. 2022;15: 100303. https://doi.org/10.1016/j.mtbio.2022.100303 .
Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010;11:785–97.
Leavesley DI, Kashyap AS, Croll T, Sivaramakrishnan M, Shokoohmand A, Hollier BG, et al. Vitronectin—master controller or micromanager? IUBMB Life. 2013;65:807–18.
Ma YJ, Garred P. Pentraxins in complement activation and regulation. Front Immunol. 2018;9:1–8.
Galván-Peña S, Carroll RG, Newman C, Hinchy EC, Palsson-McDermott E, Robinson EK, et al. Malonylation of GAPDH is an inflammatory signal in macrophages. Nat Commun. 2019. https://doi.org/10.1038/s41467-018-08187-6 .
Schittek B. The multiple facets of dermcidin in cell survival and host defense. J Innate Immun. 2012;4:349–60.
Pradipta J, Mobidullah K, Subrata DK, Asru SK, Santanu G, Gausal KA, et al. Estriol inhibits dermcidin isoform-2 induced inflammatory cytokine expression via nitric oxide synthesis in human neutrophil. Curr Mol Med. 2018;18:672–8.
Al-Mozaini MA, Tsolaki AG, Abdul-Aziz M, Abozaid SM, Al-Ahdal MN, Pathan AA, et al. Human properdin modulates macrophage: Mycobacterium bovis BCG interaction via thrombospondin repeats 4 and 5. Front Immunol. 2018;9:1–17.
Conover CA, Clarkson JT, Bale LK. Insulin-like growth factor-II enhancement of human fibroblast growth via a nonreceptor-mediated mechanism. Endocrinology. 1994;135:76–82. https://doi.org/10.1210/endo.135.1.8013394 .
Smith YE, Toomey S, Napoletano S, Kirwan G, Schadow C, Chubb AJ, et al. Recombinant PAPP-A resistant insulin-like growth factor binding protein 4 (dBP4) inhibits angiogenesis and metastasis in a murine model of breast cancer. BMC Cancer. 2018;18:1–12.
Renier G, Clément I, Desfaits A-C, Lambert A. Direct stimulatory effect of insulin-like growth factor-I on monocyte and macrophage tumor necrosis factor-α production. Endocrinology. 1996;137:4611–8.
Du L, Lin L, Li Q, Liu K, Huang Y, Wang X, et al. IGF-2 preprograms maturing macrophages to acquire oxidative phosphorylation-dependent anti-inflammatory properties. Cell Metab. 2019;29:1363-1375.e8. https://doi.org/10.1016/j.cmet.2019.01.006 .
Norseen J, Hosooka T, Hammarstedt A, Yore MM, Kant S, Aryal P, et al. Retinol-binding protein 4 inhibits insulin signaling in adipocytes by inducing proinflammatory cytokines in macrophages through a c-Jun N-terminal kinase- and toll-like receptor 4-dependent and retinol-independent mechanism. Mol Cell Biol. 2012;32:2010–9. https://doi.org/10.1128/MCB.06193-11 .
Williams DF. Titanium for medical applications. In: Brunette, Donald M, Tengvall P, Textor M, Thomsen P, editor. Titan Med Mater Sci Surf Sci Eng Biol Responses Med Appl. Berlin: Springer; 2001. p. 12–24
Bekassy Z, Lopatko Fagerström I, Bader M, Karpman D. Crosstalk between the renin–angiotensin, complement and kallikrein–kinin systems in inflammation. Nat Rev Immunol. 2022;22:411–28.
Schuijt TJ, Bakhtiari K, Daffre S, Deponte K, Wielders SJH, Marquart JA, et al. Factor XA activation of factor v is of paramount importance in initiating the coagulation system: lessons from a tick salivary protein. Circulation. 2013;128:254–66.
Miles LA, Ny L, Wilczynska M, Shen Y, Ny T, Parmer RJ. Plasminogen receptors and fibrinolysis. Int J Mol Sci. 2021;22:1–12.
Neering SH, Adyani-Fard S, Klocke A, Rüttermann S, Flemmig TF, Beikler T. Periodontitis associated with plasminogen deficiency: a case report. BMC Oral Health. 2015;15:1–12.