Top

Clinical Oral Investigations

Published in:

01-04-2021 | Original Article

Evaluating protein binding specificity of titanium surfaces through mass spectrometry–based proteomics

Authors: David Zuanazzi, Yizhi Xiao, Walter L. Siqueira

Published in: Clinical Oral Investigations | Issue 4/2021

Abstract

Objectives

To evaluate whether surface characteristics of different titanium modifications may influence the composition of the salivary pellicle on each surface by analyzing the salivary proteome through mass spectrometry–based proteomics.

Materials and methods

Titanium discs with three surfaces modifications (PT (machined titanium), SLA (sandblasted/large-grit/acid-etched), and SLActive (modified SLA)) were characterized (topography, chemistry, and energy) prior to being exposed to saliva for 2 h to form a protein pellicle. The resultant protein layer was retrieved and analyzed through mass spectrometry (nLC-ESI-MS/MS) to examine the surface specificity for protein binding, while the proteome profile of each surface was classified.

Results

The proteome analysis showed that the salivary pellicle composition was more complex on rough surfaces (SLA and SLActive). Although variability in protein composition was observed between surfaces, most proteins were detected on more than one surface, indicating a limited surface specificity for protein binding. Additionally, the salivary pellicle formed on the SLActive presented a larger number of proteins associated with immune response, biological adhesion, and biomineralization.

Conclusions

Although topography, chemistry, and energy differed between the surfaces, they were not determinant to produce a salivary pellicle with high surface specificity. Also, we showed that several salivary proteins adsorbed on Ti surfaces are involved in biological functions important to the biointegration.

Clinical relevance

This study sheds light on the necessity for the development of bioactive surfaces that favors the formation of a specific protein layer that can enhance tissue response to assist the biointegration of dental implants.

Available only for authorised users

Plecko M, Sievert C, Andermatt D, Frigg R, Kronen P, Klein K, Stubinger S, Nuss K, Burki A, Ferguson S, Stoeckle U, von Rechenberg B (2012) Osseointegration and biocompatibility of different metal implants—a comparative experimental investigation in sheep. BMC Musculoskelet Disord 13:32. https://doi.org/10.1186/1471-2474-13-32CrossRefPubMedPubMedCentral

Branemark PI (1985) Introduction to osseointegration. In: Branemark PI, Zarb GA, Albrektsson T (eds) Tissue integrated prosthesis. Quintessence International, Chicago, pp 11–76

Davies JE (1998) Mechanisms of endosseous integration. Int J Prosthodont 11(5):391–401PubMed

Ellingsen JE (1998) Surface configurations of dental implants. Periodontology 2000(17):36–46CrossRef

Puleo DA, Nanci A (1999) Understanding and controlling the bone-implant interface. Biomaterials 20(23–24):2311–2321CrossRef

Schuler M, Owen GR, Hamilton DW, de Wild M, Textor M, Brunette DM, Tosatti SG (2006) Biomimetic modification of titanium dental implant model surfaces using the RGDSP-peptide sequence: a cell morphology study. Biomaterials 27(21):4003–4015. https://doi.org/10.1016/j.biomaterials.2006.03.009CrossRefPubMed

Cooper LF (2000) A role for surface topography in creating and maintaining bone at titanium endosseous implants. J Prosthet Dent 84(5):522–534. https://doi.org/10.1067/mpr.2000.111966CrossRefPubMed

Le Guehennec L, Soueidan A, Layrolle P, Amouriq Y (2007) Surface treatments of titanium dental implants for rapid osseointegration. Dent Mater 23(7):844–854. https://doi.org/10.1016/j.dental.2006.06.025CrossRefPubMed

Cochran DL, Schenk RK, Lussi A, Higginbottom FL, Buser D (1998) Bone response to unloaded and loaded titanium implants with a sandblasted and acid-etched surface: a histometric study in the canine mandible. J Biomed Mater Res 40(1):1–11. https://doi.org/10.1002/(SICI)1097-4636(199804)40:1<1::AID-JBM1>3.0.CO;2-QCrossRefPubMed

10.

Cochran DL, Buser D, ten Bruggenkate CM, Weingart D, Taylor TM, Bernard JP, Peters F, Simpson JP (2002) The use of reduced healing times on ITI (R) implants with a sandblasted and acid-etched (SLA) surface: early results from clinical trials on ITI (R) SLA implants. Clinical Oral Implants Research 13(2):144–153. https://doi.org/10.1034/j.1600-0501.2002.130204.xCrossRefPubMed

11.

Buser D, Broggini N, Wieland M, Schenk RK, Denzer AJ, Cochran DL, Hoffmann B, Lussi A, Steinemann SG (2004) Enhanced bone apposition to a chemically modified SLA titanium surface. J Dent Res 83(7):529–533CrossRef

12.

Costa DO, Prowse PD, Chrones T, Sims SM, Hamilton DW, Rizkalla AS, Dixon SJ (2013) The differential regulation of osteoblast and osteoclast activity by surface topography of hydroxyapatite coatings. Biomaterials 34(30):7215–7226. https://doi.org/10.1016/j.biomaterials.2013.06.014CrossRefPubMed

13.

Martin JY, Schwartz Z, Hummert TW, Schraub DM, Simpson J, Lankford J Jr, Dean DD, Cochran DL, Boyan BD (1995) Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res 29(3):389–401. https://doi.org/10.1002/jbm.820290314CrossRefPubMed

14.

Rupp F, Scheideler L, Olshanska N, de Wild M, Wieland M, Geis-Gerstorfer J (2006) Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. J Biomed Mater Res A 76(2):323–334. https://doi.org/10.1002/jbm.a.30518CrossRefPubMed

15.

Biesinger MC, Lau LWM, Gerson AR, Smart RSC (2010) Resolving surface chemical states in XPS analysis of first row transition metals, oxides and hydroxides: Sc, Ti, V, cu and Zn. Appl Surf Sci 257(3):887–898. https://doi.org/10.1016/j.apsusc.2010.07.086CrossRef

16.

Siqueira WL, Bakkal M, Xiao Y, Sutton JN, Mendes FM (2012) Quantitative proteomic analysis of the effect of fluoride on the acquired enamel pellicle. PLoS One 7(8):e42204. https://doi.org/10.1371/journal.pone.0042204CrossRefPubMedPubMedCentral

17.

Zuanazzi D, Arts EJ, Jorge PK, Mulyar Y, Gibson R, Xiao Y, Bringel Dos Santos M, Machado M, Siqueira WL (2017) Postnatal identification of Zika virus peptides from saliva. J Dent Res 96(10):1078–1084. https://doi.org/10.1177/0022034517723325CrossRefPubMed

18.

Crosara KTB, Zuanazzi D, Moffa EB, Xiao Y, Machado MAdAM, Siqueira WL (2018) Revealing the amylase interactome in whole saliva using proteomic approaches. Biomed Res Int 2018:15. doi:https://doi.org/10.1155/2018/6346954, 15

19.

Oliveros JC (2007-2015) Venny. An interactive tool for comparing lists with Venn’s diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html

20.

UniProt C (2015) UniProt: a hub for protein information. Nucleic Acids Res 43(Database issue):D204–D212. https://doi.org/10.1093/nar/gku989CrossRef

21.

Dorkhan M, Chavez de Paz LE, Skepo M, Svensater G, Davies JR (2012) Effects of saliva or serum coating on adherence of Streptococcus oralis strains to titanium. Microbiology 158(Pt 2):390–397. https://doi.org/10.1099/mic.0.054536-0CrossRefPubMed

22.

Grassi S, Piattelli A, de Figueiredo LC, Feres M, de Melo L, Iezzi G, Alba RC Jr, Shibli JA (2006) Histologic evaluation of early human bone response to different implant surfaces. J Periodontol 77(10):1736–1743. https://doi.org/10.1902/jop.2006.050325CrossRefPubMed

23.

Hallab NJ, Bundy KJ, O’Connor K, Moses RL, Jacobs JJ (2001) Evaluation of metallic and polymeric biomaterial surface energy and surface roughness characteristics for directed cell adhesion. Tissue Eng 7(1):55–71. https://doi.org/10.1089/107632700300003297CrossRefPubMed

24.

Kilpadi DV, Lemons JE (1994) Surface energy characterization of unalloyed titanium implants. J Biomed Mater Res 28(12):1419–1425. https://doi.org/10.1002/jbm.820281206CrossRefPubMed

25.

Sunny MC, Sharma CP (1991) Titanium-protein interaction: changes with oxide layer thickness. J Biomater Appl 6(1):89–98. https://doi.org/10.1177/088532829100600107CrossRefPubMed

26.

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(5):630–638. https://doi.org/10.1111/j.1600-0501.2007.01373.xCrossRefPubMed

27.

Rechendorff K, Hovgaard MB, Foss M, Zhdanov VP, Besenbacher F (2006) Enhancement of protein adsorption induced by surface roughness. Langmuir : the ACS journal of surfaces and colloids 22(26):10885–10888. https://doi.org/10.1021/la0621923CrossRef

28.

Lim YJ, Oshida Y, Andres CJ, Barco MT (2001) Surface characterizations of variously treated titanium materials. Int J Oral Maxillofac Implants 16(3):333–342PubMed

29.

Rabe M, Verdes D, Seeger S (2011) Understanding protein adsorption phenomena at solid surfaces. Adv Colloid Interf Sci 162(1–2):87–106. https://doi.org/10.1016/j.cis.2010.12.007CrossRef

30.

Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ (2005) Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 11(1–2):1–18. https://doi.org/10.1089/ten.2005.11.1CrossRefPubMed

31.

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(7):e67919. https://doi.org/10.1371/journal.pone.0067919CrossRefPubMedPubMedCentral

32.

Dorkhan M, Svensater G, Davies JR (2013) Salivary pellicles on titanium and their effect on metabolic activity in Streptococcus oralis. BMC Oral Health 13:32. https://doi.org/10.1186/1472-6831-13-32CrossRefPubMedPubMedCentral

33.

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(8):780–785. https://doi.org/10.1111/j.1600-0501.2008.01524.xCrossRefPubMed

34.

Edgerton M, Lo SE, Scannapieco FA (1996) Experimental salivary pellicles formed on titanium surfaces mediate adhesion of streptococci. Int J Oral Maxillofac Implants 11(4):443–449PubMed

35.

Cavalcanti IM, 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(7):695–703. https://doi.org/10.1016/j.archoralbio.2014.04.001CrossRefPubMed

36.

Lei G, Brysk H, Arany I, Tyring SK, Srinivasan G, Brysk MM (1999) Characterization of zinc-alpha(2)-glycoprotein as a cell adhesion molecule that inhibits the proliferation of an oral tumor cell line. J Cell Biochem 75(1):160–169. https://doi.org/10.1002/(SICI)1097-4644(19991001)75:1<160::AID-JCB16>3.0.CO;2-BCrossRefPubMed

37.

Takagaki M, Honke K, Tsukamoto T, Higashiyama S, Taniguchi N, Makita A, Ohkubo I (1994) Zn-alpha 2-glycoprotein is a novel adhesive protein. Biochem Biophys Res Commun 201(3):1339–1347. https://doi.org/10.1006/bbrc.1994.1851CrossRefPubMed

38.

Bax DV, Bernard SE, Lomas A, Morgan A, Humphries J, Shuttleworth CA, Humphries MJ, Kielty CM (2003) Cell adhesion to fibrillin-1 molecules and microfibrils is mediated by alpha 5 beta 1 and alpha v beta 3 integrins. J Biol Chem 278(36):34605–34616. https://doi.org/10.1074/jbc.M303159200CrossRefPubMed

39.

Ogikubo O, Maeda T, Yamane T, Ohtsuka T, Ohkubo I, Takahashi S, Ohnishi S, Matsui N (1998) Regulation of Zn-alpha2-glycoprotein-mediated cell adhesion by kininogens and their derivatives. Biochem Biophys Res Commun 252(1):257–262. https://doi.org/10.1006/bbrc.1998.9614CrossRefPubMed

40.

Tabak LA (1990) Structure and function of human salivary mucins. Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists 1(4):229–234CrossRef

41.

van Dijk IA, Beker AF, Jellema W, Nazmi K, Wu G, Wismeijer D, Krawczyk PM, Bolscher JG, Veerman EC, Stap J (2017) Histatin 1 enhances cell adhesion to titanium in an implant integration model. J Dent Res 96(4):430–436. https://doi.org/10.1177/0022034516681761CrossRefPubMed

42.

Helmerhorst EJ, Alagl AS, Siqueira WL, Oppenheim FG (2006) Oral fluid proteolytic effects on histatin 5 structure and function. Arch Oral Biol 51(12):1061–1070. https://doi.org/10.1016/j.archoralbio.2006.06.005CrossRefPubMed

43.

Siqueira WL, Lee YH, Xiao Y, Held K, Wong W (2012) Identification and characterization of histatin 1 salivary complexes by using mass spectrometry. Proteomics 12(22):3426–3435. https://doi.org/10.1002/pmic.201100665CrossRefPubMed

44.

Wickstrom C, Christersson C, Davies JR, Carlstedt I (2000) Macromolecular organization of saliva: identification of ‘insoluble’ MUC5B assemblies and non-mucin proteins in the gel phase. Biochem J 351(Pt 2):421–428CrossRef

45.

Rosch C, Kratz F, Hering T, Trautmann S, Umanskaya N, Tippkotter N, Muller-Renno C, Ulber R, Hannig M, Ziegler C (2017) Albumin-lysozyme interactions: cooperative adsorption on titanium and enzymatic activity. Colloids Surf B Biointerfaces 149:115–121. https://doi.org/10.1016/j.colsurfb.2016.09.048CrossRefPubMed

46.

Moffa EB, Machado MA, Mussi MC, Xiao Y, Garrido SS, Giampaolo ET, Siqueira WL (2015) In vitro identification of histatin 5 salivary complexes. PLoS One 10(11):e0142517. https://doi.org/10.1371/journal.pone.0142517CrossRefPubMedPubMedCentral

47.

Sgolastra F, Petrucci A, Severino M, Gatto R, Monaco A (2015) Periodontitis, implant loss and peri-implantitis. A meta-analysis. Clin Oral Implants Res 26(4):e8–e16. https://doi.org/10.1111/clr.12319

48.

Dashper SG, Pan Y, Veith PD, Chen YY, Toh EC, Liu SW, Cross KJ, Reynolds EC (2012) Lactoferrin inhibits Porphyromonas gingivalis proteinases and has sustained biofilm inhibitory activity. Antimicrob Agents Chemother 56(3):1548–1556. https://doi.org/10.1128/AAC.05100-11CrossRefPubMedPubMedCentral

49.

Wakabayashi H, Yamauchi K, Kobayashi T, Yaeshima T, Iwatsuki K, Yoshie H (2009) Inhibitory effects of lactoferrin on growth and biofilm formation of Porphyromonas gingivalis and Prevotella intermedia. Antimicrob Agents Chemother 53(8):3308–3316. https://doi.org/10.1128/AAC.01688-08CrossRefPubMedPubMedCentral

50.

Hanif A, Qureshi S, Sheikh Z, Rashid H (2017) Complications in implant dentistry. Eur J Dent 11(1):135–140. https://doi.org/10.4103/ejd.ejd_340_16CrossRefPubMedPubMedCentral

51.

Nguyen TH, Park MD, Otto M (2017) Host response to Staphylococcus epidermidis colonization and infections. Front Cell Infect Microbiol 7:90. https://doi.org/10.3389/fcimb.2017.00090CrossRefPubMedPubMedCentral

52.

MacDonald DE, Deo N, Markovic B, Stranick M, Somasundaran P (2002) Adsorption and dissolution behavior of human plasma fibronectin on thermally and chemically modified titanium dioxide particles. Biomaterials 23(4):1269–1279. https://doi.org/10.1016/S0142-9612(01)00317-9CrossRefPubMed

53.

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(5):549–557. https://doi.org/10.1080/08927014.2013.787416CrossRefPubMed

54.

Romero-Gavilan F, Gomes NC, Rodenas J, Sanchez A, Azkargorta M, Iloro I, Elortza F, Garcia Arnaez I, Gurruchaga M, Goni I, Suay J (2017) Proteome analysis of human serum proteins adsorbed onto different titanium surfaces used in dental implants. Biofouling 33(1):98–111. https://doi.org/10.1080/08927014.2016.1259414CrossRefPubMed

55.

Barros SP, Williams R, Offenbacher S, Morelli T (2016) Gingival crevicular fluid as a source of biomarkers for periodontitis. Periodontology 2000 70 (1):53–64. doi:https://doi.org/10.1111/prd.12107

56.

Cavalcanti YW, Soare RV, Leite Assis MA, Zenobio EG, Girundi FM (2015) Titanium surface roughing treatments contribute to higher interaction with salivary proteins MG2 and lactoferrin. J Contemp Dent Pract 16(2):141–146. https://doi.org/10.5005/jp-journals-10024-1651CrossRefPubMed

57.

Hou JM, Chen EY, Lin F, Lin QM, Xue Y, Lan XH, Wu M (2015) Lactoferrin induces osteoblast growth through IGF-1R. Int J Endocrinol 2015:282806–282809. https://doi.org/10.1155/2015/282806CrossRefPubMedPubMedCentral

58.

Cornish J (2004) Lactoferrin promotes bone growth. Biometals 17(3):331–335. https://doi.org/10.1023/B:BIOM.0000027713.18694.91CrossRefPubMed

59.

Hou JM, Chen EY, Wei SC, Lin F, Lin QM, Lan XH, Xue Y, Wu M (2014) Lactoferrin inhibits apoptosis through insulin-like growth factor I in primary rat osteoblasts. Acta Pharmacol Sin 35(4):523–530. https://doi.org/10.1038/aps.2013.173CrossRefPubMedPubMedCentral

60.

Weinberg ED (2001) Human lactoferrin: a novel therapeutic with broad spectrum potential. J Pharm Pharmacol 53(10):1303–1310. https://doi.org/10.1211/0022357011777792CrossRefPubMed

61.

Manninen O, Puolakkainen T, Lehto J, Harittu E, Kallonen A, Peura M, Laitala-Leinonen T, Kopra O, Kiviranta R, Lehesjoki AE (2015) Impaired osteoclast homeostasis in the cystatin B-deficient mouse model of progressive myoclonus epilepsy. Bone Rep 3:76–82. https://doi.org/10.1016/j.bonr.2015.10.002CrossRefPubMedPubMedCentral

62.

Laitala-Leinonen T, Rinne R, Saukko P, Vaananen HK, Rinne A (2006) Cystatin B as an intracellular modulator of bone resorption. Matrix Biol 25(3):149–157. https://doi.org/10.1016/j.matbio.2005.10.005CrossRefPubMed

63.

Brage M, Abrahamson M, Lindstrom V, Grubb A, Lerner UH (2005) Different cysteine proteinases involved in bone resorption and osteoclast formation. Calcif Tissue Int 76(6):439–447. https://doi.org/10.1007/s00223-004-0043-yCrossRefPubMed

64.

Littlewood-Evans A, Kokubo T, Ishibashi O, Inaoka T, Wlodarski B, Gallagher JA, Bilbe G (1997) Localization of cathepsin K in human osteoclasts by in situ hybridization and immunohistochemistry. Bone 20(2):81–86. https://doi.org/10.1016/S8756-3282(96)00351-1CrossRefPubMed

65.

Zreiqat H, Howlett CR, Gronthos S, Hume D, Geczy CL (2007) S100A8/S100A9 and their association with cartilage and bone. J Mol Histol 38(5):381–391. https://doi.org/10.1007/s10735-007-9117-2CrossRefPubMed

66.

Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C (1997) Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem 272(14):9496–9502. https://doi.org/10.1074/jbc.272.14.9496CrossRefPubMed

67.

Zreiqat H, Belluoccio D, Smith MM, Wilson R, Rowley LA, Jones K, Ramaswamy Y, Vogl T, Roth J, Bateman JF, Little CB (2010) S100A8 and S100A9 in experimental osteoarthritis. Arthritis Res Ther 12(1):R16. https://doi.org/10.1186/ar2917CrossRefPubMedPubMedCentral

68.

Grevers LC, de Vries TJ, Vogl T, Abdollahi-Roodsaz S, Sloetjes AW, Leenen PJ, Roth J, Everts V, van den Berg WB, van Lent PL (2011) S100A8 enhances osteoclastic bone resorption in vitro through activation of toll-like receptor 4: implications for bone destruction in murine antigen-induced arthritis. Arthritis Rheum 63(5):1365–1375. https://doi.org/10.1002/art.30290CrossRefPubMed

69.

Kojima T, Andersen E, Sanchez JC, Wilkins MR, Hochstrasser DF, Pralong WF, Cimasoni G (2000) Human gingival crevicular fluid contains MRP8 (S100A8) and MRP14 (S100A9), two calcium-binding proteins of the S100 family. J Dent Res 79(2):740–747. https://doi.org/10.1177/00220345000790020701CrossRefPubMed

70.

Lundy FT, Chalk R, Lamey PJ, Shaw C, Linden GJ (2001) Quantitative analysis of MRP-8 in gingival crevicular fluid in periodontal health and disease using microbore HPLC. J Clin Periodontol 28(12):1172–1177. https://doi.org/10.1034/j.1600-051X.2001.281213.xCrossRefPubMed

Title: Evaluating protein binding specificity of titanium surfaces through mass spectrometry–based proteomics
Authors: David Zuanazzi
Yizhi Xiao
Walter L. Siqueira
Publication date: 01-04-2021
Publisher: Springer Berlin Heidelberg
Published in: Clinical Oral Investigations / Issue 4/2021
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-020-03548-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Evaluating protein binding specificity of titanium surfaces through mass spectrometry–based proteomics

Abstract

Objectives

Materials and methods

Results

Conclusions

Clinical relevance

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Materials and methods

Results

Conclusions

Clinical relevance

Please log in to get access to this content

Other articles of this Issue 4/2021

Effects of air-abrasion pressure on mechanical and bonding properties of translucent zirconia

Adipokines and periodontal markers as risk indicators of early rheumatoid arthritis: a cross-sectional study

Oral leukoplakia—epidemiological survey and histochemical analysis of 107 cases in Brazil

Effect of St. John’s wort oil and olive oil on the postoperative complications after third molar surgery: randomized, double-blind clinical trial

Anatomical analysis of mandibular posterior teeth for endodontic microsurgery: a cone-beam computed tomographic evaluation

Cytotoxic effects of submicron- and nano-scale titanium debris released from dental implants: an integrative review