Skip to main content
Top
Published in: Clinical Oral Investigations 9/2015

01-12-2015 | Original Article

Differentiation, apoptosis, and GM-CSF receptor expression of human gingival fibroblasts on a titanium surface treated by a dual acid-etched procedure

Authors: Luca Ramaglia, Gaetano Di Spigna, Gabriele Capece, Carolina Sbordone, Salvatore Salzano, Loredana Postiglione

Published in: Clinical Oral Investigations | Issue 9/2015

Login to get access

Abstract

Objectives

Analysis of the effects of titanium surface properties on the biological behavior of human gingival fibroblasts (HGFs).

Materials and methods

HGFs were in vitro cultured on a titanium surface modified by a dual acid-etched procedure and on a control machined surface. Cell adhesion, proliferation, apoptosis, production of certain extracellular matrix (ECM) proteins, and expression of granulocyte macrophage-colony stimulating factor receptor (GM-CSFR) were investigated using in each experiment a total of 18 samples for each titanium surface.

Results

Cell attachment at 3 h of culture was statistically significantly higher on the etched surface. HGF growth increased on both surfaces during the entire experimental period and at day 14 of culture cell proliferation was statistically significantly higher on the treated surface than on the control. No statistically significant differences in percentage of apoptosis events were observed between the surfaces. ECM protein production increased progressively over time on both surfaces. A statistically significant deposition was observed at day 7 and 14 for collagen I and only at day 14 for fibronectin and tenascin, when compared to the baseline. GM-CSFR registered a positive expression on both surfaces, statistically significant at day 14 on the etched surface in comparison with the machined one.

Conclusions

Data showed that titanium surface microtopography modulates in vitro cell response and phenotypical expression of HGFs. The etched surface promoted a higher cell proliferation and differentiation improving the biological behavior of HGFs.

Clinical relevance

Results suggest a possible beneficial effect of surface etching modification on peri-implant biological integration and soft tissue healing which is critical for the formation of a biological seal around the neck of dental implants.
Literature
1.
2.
go back to reference Shalabi MM, Gortemaker A, Van’t Hof MA, Jansen JA et al (2006) Implant surface roughness and bone healing: a systematic review. J Dent Res 85:496–500CrossRefPubMed Shalabi MM, Gortemaker A, Van’t Hof MA, Jansen JA et al (2006) Implant surface roughness and bone healing: a systematic review. J Dent Res 85:496–500CrossRefPubMed
3.
go back to reference Chappuis V, Buser R, Brägger U, Bornstein MM et al (2013) Long-term outcomes of dental implants with a titanium plasma-sprayed surface: a 20-year prospective case series study in partially edentulous patients. Clin Implant Dent Relat Res 15:780–790CrossRefPubMed Chappuis V, Buser R, Brägger U, Bornstein MM et al (2013) Long-term outcomes of dental implants with a titanium plasma-sprayed surface: a 20-year prospective case series study in partially edentulous patients. Clin Implant Dent Relat Res 15:780–790CrossRefPubMed
4.
go back to reference Esposito M, Maghaireh H, Grusovin MG, Ziounas I et al (2012) Soft tissue management for dental implants: what are the most effective techniques? A Cochrane systematic review. Eur J Oral Implantol 5:221–238PubMed Esposito M, Maghaireh H, Grusovin MG, Ziounas I et al (2012) Soft tissue management for dental implants: what are the most effective techniques? A Cochrane systematic review. Eur J Oral Implantol 5:221–238PubMed
5.
go back to reference Lavelle CL (1981) Mucosal seal around endosseous dental implants. J Oral Implantol 9:357–371PubMed Lavelle CL (1981) Mucosal seal around endosseous dental implants. J Oral Implantol 9:357–371PubMed
6.
go back to reference Tomasi C, Tessarolo F, Caola I, Wennström J et al (2013) Morphogenesis of peri-implant mucosa revisited: an experimental study in humans. Clin Oral Implants Res. doi:10.1111/clr.12223 Tomasi C, Tessarolo F, Caola I, Wennström J et al (2013) Morphogenesis of peri-implant mucosa revisited: an experimental study in humans. Clin Oral Implants Res. doi:10.​1111/​clr.​12223
8.
go back to reference Chavrier C, Hartmann DJ, Couble ML, Herbage D (1988) Distribution and organization of the elastic system fibres in healthy human gingiva. Ultrastructural and immunohistochemical study. Histochemistry 89:47–52CrossRefPubMed Chavrier C, Hartmann DJ, Couble ML, Herbage D (1988) Distribution and organization of the elastic system fibres in healthy human gingiva. Ultrastructural and immunohistochemical study. Histochemistry 89:47–52CrossRefPubMed
9.
go back to reference Hynes RO, Yamada KM (1982) Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95:369–377CrossRefPubMed Hynes RO, Yamada KM (1982) Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95:369–377CrossRefPubMed
10.
go back to reference Jones FS, Jones PL (2000) The Tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235–259CrossRefPubMed Jones FS, Jones PL (2000) The Tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235–259CrossRefPubMed
11.
go back to reference Schroeder HE, Listgarten MA (1997) The gingival tissues: the architecture of periodontal protection. Periodontol 2000(13):91–120CrossRef Schroeder HE, Listgarten MA (1997) The gingival tissues: the architecture of periodontal protection. Periodontol 2000(13):91–120CrossRef
12.
go back to reference Fleetwood AJ, Cook AD, Hamilton JA (2005) Functions of granulocyte-macrophage colony-stimulating factor. Crit Rev Immunol 25:405–428CrossRefPubMed Fleetwood AJ, Cook AD, Hamilton JA (2005) Functions of granulocyte-macrophage colony-stimulating factor. Crit Rev Immunol 25:405–428CrossRefPubMed
14.
go back to reference Postiglione L, Montagnani S, Riccio A, Montuori N et al (2002) Enhanced expression of the receptor for granulocyte macrophage colony stimulating factor on dermal fibroblasts from scleroderma patients. J Rheumatol 29:94–101PubMed Postiglione L, Montagnani S, Riccio A, Montuori N et al (2002) Enhanced expression of the receptor for granulocyte macrophage colony stimulating factor on dermal fibroblasts from scleroderma patients. J Rheumatol 29:94–101PubMed
15.
go back to reference Postiglione L, Di Domenico G, Montagnani S, Di Spigna G et al (2003) Granulocyte-macrophage colony-stimulating (GM-CSF) induces the osteoblastic differentiation of the human osteosarcoma cell line SaOS-2. Calcif Tissue Int 72:85–97CrossRefPubMed Postiglione L, Di Domenico G, Montagnani S, Di Spigna G et al (2003) Granulocyte-macrophage colony-stimulating (GM-CSF) induces the osteoblastic differentiation of the human osteosarcoma cell line SaOS-2. Calcif Tissue Int 72:85–97CrossRefPubMed
16.
go back to reference Di Domenico G, Del Vecchio L, Ramaglia L, Postiglione L (2003) Immunophenotipic analysis of human gingival fibroblasts and its regulation by granulocyte-macrophage colony stimulating factor (GM-CSF). Minerva Stomatol 52:81–91PubMed Di Domenico G, Del Vecchio L, Ramaglia L, Postiglione L (2003) Immunophenotipic analysis of human gingival fibroblasts and its regulation by granulocyte-macrophage colony stimulating factor (GM-CSF). Minerva Stomatol 52:81–91PubMed
17.
go back to reference Davies JE (1998) Mechanisms of endosseous integration. Int J Prosthodont 11:391–401PubMed Davies JE (1998) Mechanisms of endosseous integration. Int J Prosthodont 11:391–401PubMed
18.
go back to reference Szmukler-Moncler S, Testori T, Bernard JP (2004) Etched implants: a comparative surface analysis of four implant systems. J Biomed Mater Res B Appl Biomater 69:46–57CrossRefPubMed Szmukler-Moncler S, Testori T, Bernard JP (2004) Etched implants: a comparative surface analysis of four implant systems. J Biomed Mater Res B Appl Biomater 69:46–57CrossRefPubMed
19.
go back to reference Brunette DM (1988) The effects of implant surface topography on the behaviour of cells. Int J Oral Maxillofac Implants 3:231–246PubMed Brunette DM (1988) The effects of implant surface topography on the behaviour of cells. Int J Oral Maxillofac Implants 3:231–246PubMed
20.
go back to reference Anselme K, Bigerelle M, Noel B, Dufresne E et al (2000) Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. J Biomed Mater Res 49:155–166CrossRefPubMed Anselme K, Bigerelle M, Noel B, Dufresne E et al (2000) Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. J Biomed Mater Res 49:155–166CrossRefPubMed
21.
go back to reference Ramaglia L, Postiglione L, Di Spigna G, Capece G et al (2011) Sandblasted-acid-etched titanium surface influences in vitro the biological behavior of SaOS-2 human osteoblast-like cells. Dent Mater J 30:183–192CrossRefPubMed Ramaglia L, Postiglione L, Di Spigna G, Capece G et al (2011) Sandblasted-acid-etched titanium surface influences in vitro the biological behavior of SaOS-2 human osteoblast-like cells. Dent Mater J 30:183–192CrossRefPubMed
22.
go back to reference Palaiologou A, Stoute D, Fan Y, Lallier TE (2012) Altered cell motility and attachment with titanium surface modifications. J Periodontol 83:90–100CrossRefPubMed Palaiologou A, Stoute D, Fan Y, Lallier TE (2012) Altered cell motility and attachment with titanium surface modifications. J Periodontol 83:90–100CrossRefPubMed
23.
go back to reference Lowenberg BF, Pilliar RM, Aubin JE, Fernie GR et al (1987) Migration, attachment, and orientation of human gingival fibroblasts to root slices, naked and porous-surfaced titanium alloy discs and zircalloy-2 discs in vitro. J Dent Res 66:1000–1005CrossRefPubMed Lowenberg BF, Pilliar RM, Aubin JE, Fernie GR et al (1987) Migration, attachment, and orientation of human gingival fibroblasts to root slices, naked and porous-surfaced titanium alloy discs and zircalloy-2 discs in vitro. J Dent Res 66:1000–1005CrossRefPubMed
24.
go back to reference Guy SC, McQuade MJ, Scheidt MJ, McPherson JC III et al (1993) In vitro attachment of human gingival fibroblasts to endosseous implant materials. J Periodontol 64:542–546CrossRefPubMed Guy SC, McQuade MJ, Scheidt MJ, McPherson JC III et al (1993) In vitro attachment of human gingival fibroblasts to endosseous implant materials. J Periodontol 64:542–546CrossRefPubMed
25.
go back to reference Abrahamsson I, Zitzmann NU, Berglundh T, Wennerberg A et al (2001) Bone and soft tissue integration to titanium implants with different surface topography: an experimental study in the dog. Int J Oral Maxillofac Implants 16:323–332PubMed Abrahamsson I, Zitzmann NU, Berglundh T, Wennerberg A et al (2001) Bone and soft tissue integration to titanium implants with different surface topography: an experimental study in the dog. Int J Oral Maxillofac Implants 16:323–332PubMed
26.
go back to reference Abrahamsson I, Zitzmann NU, Berglundh T, Linder E et al (2002) The mucosal attachment to titanium implants with different surface characteristics: an experimental study in dogs. J Clin Periodontol 29:448–455CrossRefPubMed Abrahamsson I, Zitzmann NU, Berglundh T, Linder E et al (2002) The mucosal attachment to titanium implants with different surface characteristics: an experimental study in dogs. J Clin Periodontol 29:448–455CrossRefPubMed
27.
go back to reference Berglundh T, Lindhe J, Ericsson I, Marinello CP et al (1991) The soft tissue barrier at implants and teeth. Clin Oral Implants Res 2:81–90CrossRefPubMed Berglundh T, Lindhe J, Ericsson I, Marinello CP et al (1991) The soft tissue barrier at implants and teeth. Clin Oral Implants Res 2:81–90CrossRefPubMed
28.
go back to reference Listgarten MA, Lang NP, Schroeder HE, Scheroeder A (1991) Periodontal tissues and their counterparts around endosseous implants. Clin Oral Implants Res 2:1–19CrossRefPubMed Listgarten MA, Lang NP, Schroeder HE, Scheroeder A (1991) Periodontal tissues and their counterparts around endosseous implants. Clin Oral Implants Res 2:1–19CrossRefPubMed
29.
go back to reference Berglundh T, Lindhe J (1996) Dimension of the peri-implant mucosa. Biological width revisited. J Clin Periodontol 23:971–973CrossRefPubMed Berglundh T, Lindhe J (1996) Dimension of the peri-implant mucosa. Biological width revisited. J Clin Periodontol 23:971–973CrossRefPubMed
30.
go back to reference Lindhe J, Berglundh T (1998) The interface between the mucosa and the implant. J Periodontol 17:47–54CrossRef Lindhe J, Berglundh T (1998) The interface between the mucosa and the implant. J Periodontol 17:47–54CrossRef
31.
go back to reference Schupbach P, Glauser R (2007) The defense architecture of the human peri-implant mucosa: a histological study. J Prosthet Dent 97:S15–S25CrossRefPubMed Schupbach P, Glauser R (2007) The defense architecture of the human peri-implant mucosa: a histological study. J Prosthet Dent 97:S15–S25CrossRefPubMed
32.
go back to reference Kononen M, Hormia M, Kivilahti J, Hautaniemi J et al (1992) Effect of surface processing on the attachment, orientation, and proliferation of human gingival fibroblasts on titanium. J Biomed Mater Res 26:1325–1341CrossRefPubMed Kononen M, Hormia M, Kivilahti J, Hautaniemi J et al (1992) Effect of surface processing on the attachment, orientation, and proliferation of human gingival fibroblasts on titanium. J Biomed Mater Res 26:1325–1341CrossRefPubMed
33.
go back to reference Kunzler TP, Drobek T, Schuler M, Spencer ND (2007) Systematic study of osteoblast and fibroblast response to roughness by means of surface-morphology gradients. Biomaterials 28:2175–2182CrossRefPubMed Kunzler TP, Drobek T, Schuler M, Spencer ND (2007) Systematic study of osteoblast and fibroblast response to roughness by means of surface-morphology gradients. Biomaterials 28:2175–2182CrossRefPubMed
34.
go back to reference Oates TW, Maller SC, West J, Steffensen B (2005) Human gingival fibroblast integrin subunit expression on titanium implant surfaces. J Periodontol 76:1743–1750CrossRefPubMed Oates TW, Maller SC, West J, Steffensen B (2005) Human gingival fibroblast integrin subunit expression on titanium implant surfaces. J Periodontol 76:1743–1750CrossRefPubMed
35.
go back to reference Grossner-Schreiber B, Herzog M, Hedderich J, Duck A et al (2006) Focal adhesion contact formation by fibroblasts cultured on surface modified dental implants: an in vitro study. Clin Oral Implants Res 17:736–745CrossRefPubMed Grossner-Schreiber B, Herzog M, Hedderich J, Duck A et al (2006) Focal adhesion contact formation by fibroblasts cultured on surface modified dental implants: an in vitro study. Clin Oral Implants Res 17:736–745CrossRefPubMed
36.
go back to reference Albrektsson T, Wennerberg A (2004) Oral implant surfaces: part 1-review focusing on topographic and chemical properties of different surfaces and in vivo responses to them. Int J Prosthodont 17:536–543PubMed Albrektsson T, Wennerberg A (2004) Oral implant surfaces: part 1-review focusing on topographic and chemical properties of different surfaces and in vivo responses to them. Int J Prosthodont 17:536–543PubMed
37.
go back to reference Wennerberg A, Albrektsson T (2010) On implant surfaces: a review of current knowledge and opinions. Int J Oral Maxillofac Implants 25:63–74PubMed Wennerberg A, Albrektsson T (2010) On implant surfaces: a review of current knowledge and opinions. Int J Oral Maxillofac Implants 25:63–74PubMed
38.
go back to reference Postiglione L, Di Domenico G, Ramaglia L, Montagnani S et al (2003) Behavior of SaOS-2 cells cultured on different titanium surfaces. J Dent Res 82:692–696CrossRefPubMed Postiglione L, Di Domenico G, Ramaglia L, Montagnani S et al (2003) Behavior of SaOS-2 cells cultured on different titanium surfaces. J Dent Res 82:692–696CrossRefPubMed
39.
go back to reference Postiglione L, Di Domenico G, Ramaglia L, Di Lauro AE et al (2004) Different titanium surfaces modulate the bone phenotype of SaOS-2 osteoblast-like cells. Eur J Histochem 48:213–222PubMed Postiglione L, Di Domenico G, Ramaglia L, Di Lauro AE et al (2004) Different titanium surfaces modulate the bone phenotype of SaOS-2 osteoblast-like cells. Eur J Histochem 48:213–222PubMed
40.
go back to reference Wirth C, Comte V, Lagneau C (2005) Nitinol surface roughness modulates in vitro cell response: a comparison between fibroblasts and osteoblasts. Mater Sci Eng C 25:51–60CrossRef Wirth C, Comte V, Lagneau C (2005) Nitinol surface roughness modulates in vitro cell response: a comparison between fibroblasts and osteoblasts. Mater Sci Eng C 25:51–60CrossRef
41.
go back to reference Asano Y, Ihn H, Yamane K, Kubo M et al (2004) Impaired Smad7-Smurf-mediated negative regulation of TGF-β signaling in scleroderma fibroblasts. J Clin Invest 113:253–264PubMedCentralCrossRefPubMed Asano Y, Ihn H, Yamane K, Kubo M et al (2004) Impaired Smad7-Smurf-mediated negative regulation of TGF-β signaling in scleroderma fibroblasts. J Clin Invest 113:253–264PubMedCentralCrossRefPubMed
42.
go back to reference Holmes A, Abraham DJ, Sa S, Shiwen X et al (2001) CTGF and SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J Biol Chem 14:10594–10601CrossRef Holmes A, Abraham DJ, Sa S, Shiwen X et al (2001) CTGF and SMADs, maintenance of scleroderma phenotype is independent of SMAD signaling. J Biol Chem 14:10594–10601CrossRef
43.
go back to reference Mori Y, Chen SJ, Varga J (2003) Expression and regulation of intracellular SMAD signaling in scleroderma skin fibroblasts. Arthritis Rheum 48:1964–1978CrossRefPubMed Mori Y, Chen SJ, Varga J (2003) Expression and regulation of intracellular SMAD signaling in scleroderma skin fibroblasts. Arthritis Rheum 48:1964–1978CrossRefPubMed
44.
go back to reference Zetterqvist L, Feldman S, Rotter B, Vincenzi G et al (2010) A prospective, multicenter, randomized-controlled 5-year study of hybrid and fully etched implants for the incidence of peri-implantitis. J Periodontol 81:493–501CrossRefPubMed Zetterqvist L, Feldman S, Rotter B, Vincenzi G et al (2010) A prospective, multicenter, randomized-controlled 5-year study of hybrid and fully etched implants for the incidence of peri-implantitis. J Periodontol 81:493–501CrossRefPubMed
45.
go back to reference Rodriguez y Baena R, Arciola CR, Selan L, Battaglia R et al (2012) Evaluation of bacterial adhesion on machined titanium, Osseotite® and Nanotite® discs. Int J Artif Organs 35:754–761PubMed Rodriguez y Baena R, Arciola CR, Selan L, Battaglia R et al (2012) Evaluation of bacterial adhesion on machined titanium, Osseotite® and Nanotite® discs. Int J Artif Organs 35:754–761PubMed
46.
go back to reference Ramaglia L, Sbordone L, Ciaglia R, Barone A et al (1999) A clinical comparison of the efficacy and efficiency of two professional prophylaxis procedures in orthodontic patients. Eur J Orthod 21:423–428CrossRefPubMed Ramaglia L, Sbordone L, Ciaglia R, Barone A et al (1999) A clinical comparison of the efficacy and efficiency of two professional prophylaxis procedures in orthodontic patients. Eur J Orthod 21:423–428CrossRefPubMed
47.
go back to reference Ramaglia L, di Lauro AE, Morgese F, Squillace A (2006) Profilometric and standard error of the mean analysis of rough implant surfaces treated with different instrumentations. Implant Dent 15:77–82CrossRefPubMed Ramaglia L, di Lauro AE, Morgese F, Squillace A (2006) Profilometric and standard error of the mean analysis of rough implant surfaces treated with different instrumentations. Implant Dent 15:77–82CrossRefPubMed
48.
go back to reference Yeo IS, Kim HY, Lim KS, Han JS (2012) Implant surface factors and bacterial adhesion: a review of the literature. Int J Artif Organs 35:762–772CrossRefPubMed Yeo IS, Kim HY, Lim KS, Han JS (2012) Implant surface factors and bacterial adhesion: a review of the literature. Int J Artif Organs 35:762–772CrossRefPubMed
49.
go back to reference Stach RM, Kohles SS (2003) A meta-analysis examining the clinical survivability of machined-surface Osseotite implants in poor-quality bone. Implant Dent 12:87–96CrossRefPubMed Stach RM, Kohles SS (2003) A meta-analysis examining the clinical survivability of machined-surface Osseotite implants in poor-quality bone. Implant Dent 12:87–96CrossRefPubMed
50.
go back to reference Toti P, Sbordone C, Martuscelli R, Califano L et al (2013) Gene clustering analysis in human osteoporosis disease and modifications of the jawbone. Arch Oral Biol 58:912–929CrossRefPubMed Toti P, Sbordone C, Martuscelli R, Califano L et al (2013) Gene clustering analysis in human osteoporosis disease and modifications of the jawbone. Arch Oral Biol 58:912–929CrossRefPubMed
51.
go back to reference Ramaglia L, Morgese F, Filippella M, Colao A (2007) Oral and maxillofacial manifestations of Gardner’s syndrome associated with growth hormone deficiency: case report and literature review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 103:e30–34 Ramaglia L, Morgese F, Filippella M, Colao A (2007) Oral and maxillofacial manifestations of Gardner’s syndrome associated with growth hormone deficiency: case report and literature review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 103:e30–34
52.
go back to reference Sullivan D, Sherwood R, Porter S (2001) Long-term performance of Osseotite implants: a 6-year clinical follow-up. Compend Contin Educ Dent 22:326–334PubMed Sullivan D, Sherwood R, Porter S (2001) Long-term performance of Osseotite implants: a 6-year clinical follow-up. Compend Contin Educ Dent 22:326–334PubMed
Metadata
Title
Differentiation, apoptosis, and GM-CSF receptor expression of human gingival fibroblasts on a titanium surface treated by a dual acid-etched procedure
Authors
Luca Ramaglia
Gaetano Di Spigna
Gabriele Capece
Carolina Sbordone
Salvatore Salzano
Loredana Postiglione
Publication date
01-12-2015
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 9/2015
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-015-1469-5

Other articles of this Issue 9/2015

Clinical Oral Investigations 9/2015 Go to the issue