Skip to main content
Erschienen in: Clinical Oral Investigations 4/2016

14.08.2015 | Original Article

Enamel matrix derivative improves gingival fibroblast cell behavior cultured on titanium surfaces

verfasst von: Yulan Wang, Yufeng Zhang, Dai Jing, Yang Shuang, Richard J. Miron

Erschienen in: Clinical Oral Investigations | Ausgabe 4/2016

Einloggen, um Zugang zu erhalten

Abstract

Objective

Although an extensive amount of research has demonstrated the positive effects of an enamel matrix derivative (EMD) on soft tissue wound healing around intrabony defects, little information is available describing its effect on peri-implant soft tissues, an area that has recently gained tremendous awareness due to the increasing prevalence of peri-implantitis. The aim of the present study was to assess the role of EMD when gingival fibroblasts were cultured on titanium surface with different surface topographies.

Methods

Human primary gingival fibroblasts were cultured on pickled (PT) and sand-blasted with large grit followed by acid etching (SLA) surfaces and assessed for cell adhesion at 2, 4, and 8 h, cell morphology at 2, 4, 8, and 24 h as well as cell proliferation at 1, 3, and 5 days post-seeding. Furthermore, genes encoding collagen 1a1, vascular endothelial growth factor-A (VEGF-A), and fibronectin were assessed by real-time PCR. Human gingival fibroblasts were also quantified for their ability to synthesize a collagen matrix on the various titanium surfaces with and without EMD by immunofluorescence staining.

Results

The results from the present study demonstrate that EMD significantly increased cell spreading at 2, 4, 8, and 24 h on PT surfaces and 4, 8, and 24 h on SLA surfaces. Furthermore, proliferation at 5 days on PT surfaces and 3 and 5 days on SLA surfaces was also increased for groups containing EMD. Real-time PCR results demonstrated that the culture of gingival fibroblasts with EMD significantly increased extracellular matrix synthesis of collagen 1 as well as improved mRNA levels of VEGF-A and fibronectin. Collagen1 immuno-fluorescent staining revealed a significantly higher area of staining for cells seeded on PT + EMD at 7 and 14 days and 14 days for SLA + EMD when compared to control samples.

Conclusion

The results from the present study favor the use of EMD for colonization of gingival fibroblasts on titanium surfaces by increasing cell growth, spreading, and synthesis of an extracellular matrix. The improvements were primarily irrespective of surface topography. Future animal and human studies are necessary to fully characterize the beneficial effects of incorporating EMD during soft tissue regeneration of implant protocols.

Clinical relevance

The use of EMD may speed up the quality of soft tissue integration around dental implants by facilitating gingival cell attachment, proliferation, and matrix synthesis of collagen 1.
Literatur
1.
Zurück zum Zitat Sculean A, Alessandri R, Miron R, Salvi GE, Bosshardt DD (2011) Enamel matrix proteins and periodontal wound healing and regeneration. Clinical Advances in Periodontics 1:101–117CrossRef Sculean A, Alessandri R, Miron R, Salvi GE, Bosshardt DD (2011) Enamel matrix proteins and periodontal wound healing and regeneration. Clinical Advances in Periodontics 1:101–117CrossRef
3.
Zurück zum Zitat Margolis HC, Beniash E, Fowler CE (2006) Role of macromolecular assembly of enamel matrix proteins in enamel formation. J Dent Res 85:775–793CrossRefPubMed Margolis HC, Beniash E, Fowler CE (2006) Role of macromolecular assembly of enamel matrix proteins in enamel formation. J Dent Res 85:775–793CrossRefPubMed
5.
Zurück zum Zitat Hammarstrom L (1997) Enamel matrix, cementum development and regeneration. J Clin Periodontol 24:658–668CrossRefPubMed Hammarstrom L (1997) Enamel matrix, cementum development and regeneration. J Clin Periodontol 24:658–668CrossRefPubMed
6.
Zurück zum Zitat Slavkin HC, Bessem C, Bringas P, Zeichner‐David M, Nanci A, Snead ML (1988) Sequential expression and differential function of multiple enamel proteins during fetal, neonatal, and early postnatal stages of mouse molar organogenesis. Differentiation 37:26–39CrossRefPubMed Slavkin HC, Bessem C, Bringas P, Zeichner‐David M, Nanci A, Snead ML (1988) Sequential expression and differential function of multiple enamel proteins during fetal, neonatal, and early postnatal stages of mouse molar organogenesis. Differentiation 37:26–39CrossRefPubMed
7.
Zurück zum Zitat Slavkin HC, Bessem C, Fincham AG, Bringas P, Santos V, Snead ML, Zeichner-David M (1989) Human and mouse cementum proteins immunologically related to enamel proteins. Biochimica et Biophysica Acta (BBA)-General Subjects 991:12–18CrossRef Slavkin HC, Bessem C, Fincham AG, Bringas P, Santos V, Snead ML, Zeichner-David M (1989) Human and mouse cementum proteins immunologically related to enamel proteins. Biochimica et Biophysica Acta (BBA)-General Subjects 991:12–18CrossRef
8.
Zurück zum Zitat Lindskog S (1982) Formation of intermediate cementum. I: early mineralization of aprismatic enamel and intermediate cementum in monkey. J Craniofac Genet Dev Biol 2:147–160PubMed Lindskog S (1982) Formation of intermediate cementum. I: early mineralization of aprismatic enamel and intermediate cementum in monkey. J Craniofac Genet Dev Biol 2:147–160PubMed
9.
Zurück zum Zitat Lindskog S (1982) Formation of intermediate cementum. II: a scanning electron microscopic study of the epithelial root sheath of Hertwig in monkey. J Craniofac Genet Dev Biol 2:161–169PubMed Lindskog S (1982) Formation of intermediate cementum. II: a scanning electron microscopic study of the epithelial root sheath of Hertwig in monkey. J Craniofac Genet Dev Biol 2:161–169PubMed
10.
Zurück zum Zitat Lindskog S, Hammarstrom L (1982) Formation of intermediate cementum. III: 3H-tryptophan and 3H-proline uptake into the epithelial root sheath of Hertwig in vitro. J Craniofac Genet Dev Biol 2:171–177PubMed Lindskog S, Hammarstrom L (1982) Formation of intermediate cementum. III: 3H-tryptophan and 3H-proline uptake into the epithelial root sheath of Hertwig in vitro. J Craniofac Genet Dev Biol 2:171–177PubMed
11.
Zurück zum Zitat Heijl L (1997) Periodontal regeneration with enamel matrix derivative in one human experimental defect. A case report. J Clin Periodontol 24:693–696CrossRefPubMed Heijl L (1997) Periodontal regeneration with enamel matrix derivative in one human experimental defect. A case report. J Clin Periodontol 24:693–696CrossRefPubMed
12.
Zurück zum Zitat Heijl L, Heden G, Svärdström G, Ostgren A (1997) Enamel matrix derivative (EMDOGAIN) in the treatment of intrabony periodontal defects. J Clin Periodontol 24:705–714CrossRefPubMed Heijl L, Heden G, Svärdström G, Ostgren A (1997) Enamel matrix derivative (EMDOGAIN) in the treatment of intrabony periodontal defects. J Clin Periodontol 24:705–714CrossRefPubMed
13.
Zurück zum Zitat Gestrelius S, Andersson C, Lidström D, Hammarström L, Somerman M (1997) In vitro studies on periodontal ligament cells and enamel matrix derivative. J Clin Periodontol 24:685–692CrossRefPubMed Gestrelius S, Andersson C, Lidström D, Hammarström L, Somerman M (1997) In vitro studies on periodontal ligament cells and enamel matrix derivative. J Clin Periodontol 24:685–692CrossRefPubMed
15.
Zurück zum Zitat Sculean A, Windisch P, Keglevich T, Fabi B, Lundgren E, Lyngstadaas PS (2002) Presence of an enamel matrix protein derivative on human teeth following periodontal surgery. Clin Oral Investig 6:183–187. doi:10.1007/s00784-002-0171-6 CrossRefPubMed Sculean A, Windisch P, Keglevich T, Fabi B, Lundgren E, Lyngstadaas PS (2002) Presence of an enamel matrix protein derivative on human teeth following periodontal surgery. Clin Oral Investig 6:183–187. doi:10.​1007/​s00784-002-0171-6 CrossRefPubMed
16.
Zurück zum Zitat Miron RJ, Dard M and Weinreb M (2014) Enamel matrix derivative, inflammation and soft tissue wound healing. Journal of periodontal research. doi: 10.1111/jre.12245 Miron RJ, Dard M and Weinreb M (2014) Enamel matrix derivative, inflammation and soft tissue wound healing. Journal of periodontal research. doi: 10.​1111/​jre.​12245
17.
Zurück zum Zitat Hagewald S, Spahr A, Rompola E, Haller B, Heijl L, Bernimoulin JP (2002) Comparative study of Emdogain and coronally advanced flap technique in the treatment of human gingival recessions. A prospective controlled clinical study. J Clin Periodontol 29:35–41CrossRefPubMed Hagewald S, Spahr A, Rompola E, Haller B, Heijl L, Bernimoulin JP (2002) Comparative study of Emdogain and coronally advanced flap technique in the treatment of human gingival recessions. A prospective controlled clinical study. J Clin Periodontol 29:35–41CrossRefPubMed
18.
Zurück zum Zitat Cueva MA, Boltchi FE, Hallmon WW, Nunn ME, Rivera-Hidalgo F, Rees T (2004) A comparative study of coronally advanced flaps with and without the addition of enamel matrix derivative in the treatment of marginal tissue recession. J Periodontol 75:949–956. doi:10.1902/jop.2004.75.7.949 CrossRefPubMed Cueva MA, Boltchi FE, Hallmon WW, Nunn ME, Rivera-Hidalgo F, Rees T (2004) A comparative study of coronally advanced flaps with and without the addition of enamel matrix derivative in the treatment of marginal tissue recession. J Periodontol 75:949–956. doi:10.​1902/​jop.​2004.​75.​7.​949 CrossRefPubMed
19.
Zurück zum Zitat Tonetti MS, Fourmousis I, Suvan J, Cortellini P, Bragger U, Lang NP and European Research Group on P (2004) Healing, post-operative morbidity and patient perception of outcomes following regenerative therapy of deep intrabony defects. J Clin Periodontol 31:1092–1098. doi:10.1111/j.1600-051X.2004.00615.x CrossRef Tonetti MS, Fourmousis I, Suvan J, Cortellini P, Bragger U, Lang NP and European Research Group on P (2004) Healing, post-operative morbidity and patient perception of outcomes following regenerative therapy of deep intrabony defects. J Clin Periodontol 31:1092–1098. doi:10.​1111/​j.​1600-051X.​2004.​00615.​x CrossRef
20.
Zurück zum Zitat Nemcovsky CE, Artzi Z, Tal H, Kozlovsky A, Moses O (2004) A multicenter comparative study of two root coverage procedures: coronally advanced flap with addition of enamel matrix proteins and subpedicle connective tissue graft. J Periodontol 75:600–607. doi:10.1902/jop.2004.75.4.600 CrossRefPubMed Nemcovsky CE, Artzi Z, Tal H, Kozlovsky A, Moses O (2004) A multicenter comparative study of two root coverage procedures: coronally advanced flap with addition of enamel matrix proteins and subpedicle connective tissue graft. J Periodontol 75:600–607. doi:10.​1902/​jop.​2004.​75.​4.​600 CrossRefPubMed
22.
Zurück zum Zitat Chadwick P, Acton C (2009) The use of amelogenin protein in the treatment of hard-to-heal wounds. Br J Nurs 18:S22CrossRefPubMed Chadwick P, Acton C (2009) The use of amelogenin protein in the treatment of hard-to-heal wounds. Br J Nurs 18:S22CrossRefPubMed
23.
Zurück zum Zitat Huldt-Nystrom T, Meuleniere F, Acton C (2008) Xelma®, an advanced wound treatment for venous ulcers: a European perspective. WOUNDS UK 4:84 Huldt-Nystrom T, Meuleniere F, Acton C (2008) Xelma®, an advanced wound treatment for venous ulcers: a European perspective. WOUNDS UK 4:84
24.
Zurück zum Zitat Romanelli M (2008) Quality of life assessments with the EuroQol instrument (EQ-5D) in a clinical trial of an advanced therapy using amelogenin in patients with chronic venous leg ulcers. Romanelli M (2008) Quality of life assessments with the EuroQol instrument (EQ-5D) in a clinical trial of an advanced therapy using amelogenin in patients with chronic venous leg ulcers.
25.
Zurück zum Zitat Romanelli M, Dini V, Vowden P, Agren MS (2008) Amelogenin, an extracellular matrix protein, in the treatment of venous leg ulcers and other hard-to-heal wounds: experimental and clinical evidence. Clin Interv Aging 3:263–272PubMedPubMedCentral Romanelli M, Dini V, Vowden P, Agren MS (2008) Amelogenin, an extracellular matrix protein, in the treatment of venous leg ulcers and other hard-to-heal wounds: experimental and clinical evidence. Clin Interv Aging 3:263–272PubMedPubMedCentral
26.
Zurück zum Zitat Hampton S, Kerr A and Bree-Aslan C (2007) An evaluation of a matrix replacement treatment in intractable wounds. Hampton S, Kerr A and Bree-Aslan C (2007) An evaluation of a matrix replacement treatment in intractable wounds.
27.
Zurück zum Zitat Vowden K, Mcgowan J, Pilcher M, D’Arcy A, Renton C, Warner V, Megson J and Vowden P (2007) Experience with the use of an amelogenin-based extracellular matrix substitute in the management of a variety of complex hard-to-heal chronic wounds [poster]. Vowden K, Mcgowan J, Pilcher M, D’Arcy A, Renton C, Warner V, Megson J and Vowden P (2007) Experience with the use of an amelogenin-based extracellular matrix substitute in the management of a variety of complex hard-to-heal chronic wounds [poster].
28.
Zurück zum Zitat Vowden P, Romanelli M, Price P (2007) Effect of amelogenin extracellular matrix protein and compression on hard-to-heal venous leg ulcers. J Wound Care 16:189CrossRefPubMed Vowden P, Romanelli M, Price P (2007) Effect of amelogenin extracellular matrix protein and compression on hard-to-heal venous leg ulcers. J Wound Care 16:189CrossRefPubMed
29.
Zurück zum Zitat Vowden P, Romanelli M, Peter R, Bostrom A, Josefsson A, Stege H (2006) The effect of amelogenins (Xelma) on hard-to-heal venous leg ulcers. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society 14:240–246. doi:10.1111/j.1743-6109.2006.00117.x CrossRef Vowden P, Romanelli M, Peter R, Bostrom A, Josefsson A, Stege H (2006) The effect of amelogenins (Xelma) on hard-to-heal venous leg ulcers. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society 14:240–246. doi:10.​1111/​j.​1743-6109.​2006.​00117.​x CrossRef
30.
Zurück zum Zitat Bond E, Barrett S, Pragnell J (2009) Successful treatment of non-healing wounds with Xelma(R). British journal of nursing (Mark Allen Publishing) 18:1404–1409CrossRef Bond E, Barrett S, Pragnell J (2009) Successful treatment of non-healing wounds with Xelma(R). British journal of nursing (Mark Allen Publishing) 18:1404–1409CrossRef
31.
Zurück zum Zitat Mombelli A, Lang NP (1998) The diagnosis and treatment of peri-implantitis. Periodontology 2000 17:63–76CrossRefPubMed Mombelli A, Lang NP (1998) The diagnosis and treatment of peri-implantitis. Periodontology 2000 17:63–76CrossRefPubMed
32.
Zurück zum Zitat Renvert S, Roos‐Jansåker AM, Claffey N (2008) Non-surgical treatment of peri-implant mucositis and peri-implantitis: a literature review. J Clin Periodontol 35:305–315CrossRefPubMed Renvert S, Roos‐Jansåker AM, Claffey N (2008) Non-surgical treatment of peri-implant mucositis and peri-implantitis: a literature review. J Clin Periodontol 35:305–315CrossRefPubMed
33.
Zurück zum Zitat Lindhe J, Meyle J (2008) Peri-implant diseases: consensus report of the Sixth European Workshop on Periodontology. J Clin Periodontol 35:282–285CrossRefPubMed Lindhe J, Meyle J (2008) Peri-implant diseases: consensus report of the Sixth European Workshop on Periodontology. J Clin Periodontol 35:282–285CrossRefPubMed
34.
Zurück zum Zitat Ertugrul AS, Tekin Y, Alpaslan NZ, Bozoglan A, Sahin H, Dikilitas A (2014) Comparison of peri-implant crevicular fluid levels of adrenomedullin and human beta defensins 1 and 2 from mandibular implants with different implant stability quotient levels in nonsmoker patients. J Periodontal Res 49:480–488. doi:10.1111/jre.12127 CrossRefPubMed Ertugrul AS, Tekin Y, Alpaslan NZ, Bozoglan A, Sahin H, Dikilitas A (2014) Comparison of peri-implant crevicular fluid levels of adrenomedullin and human beta defensins 1 and 2 from mandibular implants with different implant stability quotient levels in nonsmoker patients. J Periodontal Res 49:480–488. doi:10.​1111/​jre.​12127 CrossRefPubMed
35.
Zurück zum Zitat Pirih FQ, Hiyari S, Barroso AD, Jorge AC, Perussolo J, Atti E, Tetradis S and Camargo PM (2014) Ligature-induced peri-implantitis in mice. Journal of Periodontal Research. doi: 10.1111/jre.12234 Pirih FQ, Hiyari S, Barroso AD, Jorge AC, Perussolo J, Atti E, Tetradis S and Camargo PM (2014) Ligature-induced peri-implantitis in mice. Journal of Periodontal Research. doi: 10.​1111/​jre.​12234
36.
Zurück zum Zitat John G, Sahm N, Becker J and Schwarz F (2015) Nonsurgical treatment of peri-implantitis using an air-abrasive device or mechanical debridement and local application of chlorhexidine. Twelve-month follow-up of a prospective, randomized, controlled clinical study. Clinical Oral Investigations. doi: 10.1007/s00784-015-1406-7 John G, Sahm N, Becker J and Schwarz F (2015) Nonsurgical treatment of peri-implantitis using an air-abrasive device or mechanical debridement and local application of chlorhexidine. Twelve-month follow-up of a prospective, randomized, controlled clinical study. Clinical Oral Investigations. doi: 10.​1007/​s00784-015-1406-7
37.
Zurück zum Zitat Schwarz F, Mihatovic I, Golubovic V, Becker J, Sager M (2014) Immunohistochemical characteristics of regenerated bone after surgical therapy of advanced ligature-induced peri-implantitis defects. Clin Oral Investig 18:1679–1686. doi:10.1007/s00784-013-1138-5 CrossRefPubMed Schwarz F, Mihatovic I, Golubovic V, Becker J, Sager M (2014) Immunohistochemical characteristics of regenerated bone after surgical therapy of advanced ligature-induced peri-implantitis defects. Clin Oral Investig 18:1679–1686. doi:10.​1007/​s00784-013-1138-5 CrossRefPubMed
38.
Zurück zum Zitat Branemark P-I (1983) Osseointegration and its experimental background. J Prosthet Dent 50:399–410CrossRefPubMed Branemark P-I (1983) Osseointegration and its experimental background. J Prosthet Dent 50:399–410CrossRefPubMed
39.
Zurück zum Zitat Wong M, Eulenberger J, Schenk R, Hunziker E (1995) Effect of surface topology on the osseointegration of implant materials in trabecular bone. J Biomed Mater Res 29:1567–1575CrossRefPubMed Wong M, Eulenberger J, Schenk R, Hunziker E (1995) Effect of surface topology on the osseointegration of implant materials in trabecular bone. J Biomed Mater Res 29:1567–1575CrossRefPubMed
40.
Zurück zum Zitat Buser D, Schenk RK, Steinemann S, Fiorellini JP, Fox CH, Stich H (1991) Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. J Biomed Mater Res 25:889–902CrossRefPubMed Buser D, Schenk RK, Steinemann S, Fiorellini JP, Fox CH, Stich H (1991) Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. J Biomed Mater Res 25:889–902CrossRefPubMed
41.
Zurück zum Zitat 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 83:529–533CrossRefPubMed 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 83:529–533CrossRefPubMed
42.
Zurück zum Zitat Miron RJ, Bosshardt DD, Buser D, Zhang Y, Tugulu S, Gemperli A, Dard M, Caluseru OM, Chandad F and Sculean A (2015) Comparison of the capacity of enamel matrix derivative-gel and enamel matrix derivative in liquid formulation to adsorb to bone grafting materials. Journal of Periodontology:1-18. doi: 10.1902/jop.2015.140538 Miron RJ, Bosshardt DD, Buser D, Zhang Y, Tugulu S, Gemperli A, Dard M, Caluseru OM, Chandad F and Sculean A (2015) Comparison of the capacity of enamel matrix derivative-gel and enamel matrix derivative in liquid formulation to adsorb to bone grafting materials. Journal of Periodontology:1-18. doi: 10.​1902/​jop.​2015.​140538
43.
Zurück zum Zitat Miron RJ, Bosshardt DD, Hedbom E, Zhang Y, Haenni B, Buser D, Sculean A (2012) Adsorption of enamel matrix proteins to a bovine-derived bone grafting material and its regulation of cell adhesion, proliferation, and differentiation. J Periodontol 83:936–947. doi:10.1902/jop.2011.110480 CrossRefPubMed Miron RJ, Bosshardt DD, Hedbom E, Zhang Y, Haenni B, Buser D, Sculean A (2012) Adsorption of enamel matrix proteins to a bovine-derived bone grafting material and its regulation of cell adhesion, proliferation, and differentiation. J Periodontol 83:936–947. doi:10.​1902/​jop.​2011.​110480 CrossRefPubMed
45.
Zurück zum Zitat Miron RJ, Hedbom E, Ruggiero S, Bosshardt DD, Zhang Y, Mauth C, Gemperli AC, Iizuka T, Buser D, Sculean A (2011) Premature osteoblast clustering by enamel matrix proteins induces osteoblast differentiation through up-regulation of connexin 43 and N-cadherin. PLoS One 6:e23375CrossRefPubMedPubMedCentral Miron RJ, Hedbom E, Ruggiero S, Bosshardt DD, Zhang Y, Mauth C, Gemperli AC, Iizuka T, Buser D, Sculean A (2011) Premature osteoblast clustering by enamel matrix proteins induces osteoblast differentiation through up-regulation of connexin 43 and N-cadherin. PLoS One 6:e23375CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Zhang Y, Wei L, Chang J, Miron RJ, Shi B, Yi S, Wu C (2013) Strontium-incorporated mesoporous bioactive glass scaffolds stimulating in vitro proliferation and differentiation of bone marrow stromal cells and in vivo regeneration of osteoporotic bone defects. J Mater Chem B 1:5711–5722. doi:10.1039/C3TB21047B CrossRef Zhang Y, Wei L, Chang J, Miron RJ, Shi B, Yi S, Wu C (2013) Strontium-incorporated mesoporous bioactive glass scaffolds stimulating in vitro proliferation and differentiation of bone marrow stromal cells and in vivo regeneration of osteoporotic bone defects. J Mater Chem B 1:5711–5722. doi:10.​1039/​C3TB21047B CrossRef
47.
Zurück zum Zitat Zhang Y, Wei L, Miron RJ, Shi B and Bian Z (2014) Anabolic bone formation via a site specific bone targeting delivery system by interfering with semaphorin 4D expression. Journal of Bone and Mineral Research: the official journal of the American Society for Bone and Mineral Research. doi: 10.1002/jbmr.2322 Zhang Y, Wei L, Miron RJ, Shi B and Bian Z (2014) Anabolic bone formation via a site specific bone targeting delivery system by interfering with semaphorin 4D expression. Journal of Bone and Mineral Research: the official journal of the American Society for Bone and Mineral Research. doi: 10.​1002/​jbmr.​2322
48.
Zurück zum Zitat Birang R, Shahabooei M, Mashhadiabbas F, Atabaki M, Naghsh N, Kavosh K, Birang E, Mogharehabed A (2012) Effect of enamel matrix derivative on bone formation around intraosseous titanium implant: an experimental study in canine model. Dental research journal 9:790–796PubMedPubMedCentral Birang R, Shahabooei M, Mashhadiabbas F, Atabaki M, Naghsh N, Kavosh K, Birang E, Mogharehabed A (2012) Effect of enamel matrix derivative on bone formation around intraosseous titanium implant: an experimental study in canine model. Dental research journal 9:790–796PubMedPubMedCentral
49.
Zurück zum Zitat Casati MZ, Sallum EA, Nociti FH Jr, Caffesse RG, Sallum AW (2002) Enamel matrix derivative and bone healing after guided bone regeneration in dehiscence-type defects around implants. A histomorphometric study in dogs. J Periodontol 73:789–796. doi:10.1902/jop.2002.73.7.789 CrossRefPubMed Casati MZ, Sallum EA, Nociti FH Jr, Caffesse RG, Sallum AW (2002) Enamel matrix derivative and bone healing after guided bone regeneration in dehiscence-type defects around implants. A histomorphometric study in dogs. J Periodontol 73:789–796. doi:10.​1902/​jop.​2002.​73.​7.​789 CrossRefPubMed
50.
Zurück zum Zitat Qu Z, Andrukhov O, Laky M, Ulm C, Matejka M, Dard M, Rausch-Fan X (2011) Effect of enamel matrix derivative on proliferation and differentiation of osteoblast cells grown on the titanium implant surface. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 111:517–522. doi:10.1016/j.tripleo.2010.10.011 CrossRefPubMed Qu Z, Andrukhov O, Laky M, Ulm C, Matejka M, Dard M, Rausch-Fan X (2011) Effect of enamel matrix derivative on proliferation and differentiation of osteoblast cells grown on the titanium implant surface. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 111:517–522. doi:10.​1016/​j.​tripleo.​2010.​10.​011 CrossRefPubMed
51.
Zurück zum Zitat Shimizu-Ishiura M, Tanaka S, Lee WS, Debari K, Sasaki T (2002) Effects of enamel matrix derivative to titanium implantation in rat femurs. J Biomed Mater Res 60:269–276CrossRefPubMed Shimizu-Ishiura M, Tanaka S, Lee WS, Debari K, Sasaki T (2002) Effects of enamel matrix derivative to titanium implantation in rat femurs. J Biomed Mater Res 60:269–276CrossRefPubMed
52.
Zurück zum Zitat Miron RJ, Bosshardt DD, Gemperli AC, Dard M, Buser D, Gruber R, Sculean A (2014) In vitro characterization of a synthetic calcium phosphate bone graft on periodontal ligament cell and osteoblast behavior and its combination with an enamel matrix derivative. Clin Oral Investig 18:443–451. doi:10.1007/s00784-013-0977-4 CrossRefPubMed Miron RJ, Bosshardt DD, Gemperli AC, Dard M, Buser D, Gruber R, Sculean A (2014) In vitro characterization of a synthetic calcium phosphate bone graft on periodontal ligament cell and osteoblast behavior and its combination with an enamel matrix derivative. Clin Oral Investig 18:443–451. doi:10.​1007/​s00784-013-0977-4 CrossRefPubMed
53.
Zurück zum Zitat Miron RJ, Bosshardt DD, Laugisch O, Dard M, Gemperli AC, Buser D, Gruber R, Sculean A (2013) In vitro evaluation of demineralized freeze-dried bone allograft in combination with enamel matrix derivative. J Periodontol 84:1646–1654. doi:10.1902/jop.2013.120574 PubMed Miron RJ, Bosshardt DD, Laugisch O, Dard M, Gemperli AC, Buser D, Gruber R, Sculean A (2013) In vitro evaluation of demineralized freeze-dried bone allograft in combination with enamel matrix derivative. J Periodontol 84:1646–1654. doi:10.​1902/​jop.​2013.​120574 PubMed
54.
55.
Zurück zum Zitat Hoang AM, Klebe RJ, Steffensen B, Ryu OH, Simmer JP, Cochran DL (2002) Amelogenin is a cell adhesion protein. J Dent Res 81:497–500CrossRefPubMed Hoang AM, Klebe RJ, Steffensen B, Ryu OH, Simmer JP, Cochran DL (2002) Amelogenin is a cell adhesion protein. J Dent Res 81:497–500CrossRefPubMed
58.
Zurück zum Zitat Weinberg E, Topaz M, Dard M, Lyngstadaas P, Nemcovsky C, Weinreb M (2010) Differential effects of prostaglandin E(2) and enamel matrix derivative on the proliferation of human gingival and dermal fibroblasts and gingival keratinocytes. J Periodontal Res 45:731–740. doi:10.1111/j.1600-0765.2010.01293.x CrossRefPubMed Weinberg E, Topaz M, Dard M, Lyngstadaas P, Nemcovsky C, Weinreb M (2010) Differential effects of prostaglandin E(2) and enamel matrix derivative on the proliferation of human gingival and dermal fibroblasts and gingival keratinocytes. J Periodontal Res 45:731–740. doi:10.​1111/​j.​1600-0765.​2010.​01293.​x CrossRefPubMed
59.
Zurück zum Zitat Wu SM, Chiu HC, Chin YT, Lin HY, Chiang CY, Tu HP, Fu MM, Fu E (2014) Effects of enamel matrix derivative on the proliferation and osteogenic differentiation of human gingival mesenchymal stem cells. Stem cell research & therapy 5:52. doi:10.1186/scrt441 CrossRef Wu SM, Chiu HC, Chin YT, Lin HY, Chiang CY, Tu HP, Fu MM, Fu E (2014) Effects of enamel matrix derivative on the proliferation and osteogenic differentiation of human gingival mesenchymal stem cells. Stem cell research & therapy 5:52. doi:10.​1186/​scrt441 CrossRef
60.
Zurück zum Zitat Zeldich E, Koren R, Dard M, Nemcovsky C, Weinreb M (2008) EGFR in enamel matrix derivative-induced gingival fibroblast mitogenesis. J Dent Res 87:850–855CrossRefPubMed Zeldich E, Koren R, Dard M, Nemcovsky C, Weinreb M (2008) EGFR in enamel matrix derivative-induced gingival fibroblast mitogenesis. J Dent Res 87:850–855CrossRefPubMed
61.
Zurück zum Zitat Zeldich E, Koren R, Nemcovsky C, Weinreb M (2007) Enamel matrix derivative stimulates human gingival fibroblast proliferation via ERK. J Dent Res 86:41–46CrossRefPubMed Zeldich E, Koren R, Nemcovsky C, Weinreb M (2007) Enamel matrix derivative stimulates human gingival fibroblast proliferation via ERK. J Dent Res 86:41–46CrossRefPubMed
62.
Zurück zum Zitat Ponsonnet L, Comte V, Othmane A, Lagneau C, Charbonnier M, Lissac M, Jaffrezic N (2002) Effect of surface topography and chemistry on adhesion, orientation and growth of fibroblasts on nickel–titanium substrates. Mater Sci Eng, C 21:157–165. doi:10.1016/S0928-4931(02)00097-8 CrossRef Ponsonnet L, Comte V, Othmane A, Lagneau C, Charbonnier M, Lissac M, Jaffrezic N (2002) Effect of surface topography and chemistry on adhesion, orientation and growth of fibroblasts on nickel–titanium substrates. Mater Sci Eng, C 21:157–165. doi:10.​1016/​S0928-4931(02)00097-8 CrossRef
63.
Zurück zum Zitat Martin JY, Schwartz Z, Hummert TW, Schraub DM, Simpson J, Lankford J, 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 29:389–401CrossRefPubMed Martin JY, Schwartz Z, Hummert TW, Schraub DM, Simpson J, Lankford J, 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 29:389–401CrossRefPubMed
64.
Zurück zum Zitat Chou L, Firth JD, Uitto V-J, Brunette DM (1995) Substratum surface topography alters cell shape and regulates fibronectin mRNA level, mRNA stability, secretion and assembly in human fibroblasts. J Cell Sci 108:1563–1573PubMed Chou L, Firth JD, Uitto V-J, Brunette DM (1995) Substratum surface topography alters cell shape and regulates fibronectin mRNA level, mRNA stability, secretion and assembly in human fibroblasts. J Cell Sci 108:1563–1573PubMed
65.
Zurück zum Zitat Brunette DM, Chehroudi B (1999) The effects of the surface topography of micromachined titanium substrata on cell behavior in vitro and in vivo. J Biomech Eng 121:49–57CrossRefPubMed Brunette DM, Chehroudi B (1999) The effects of the surface topography of micromachined titanium substrata on cell behavior in vitro and in vivo. J Biomech Eng 121:49–57CrossRefPubMed
66.
Zurück zum Zitat Brunette DM, Kenner GS, Gould TRL (1983) Grooved titanium surfaces orient growth and migration of cells from human gingival explants. J Dent Res 62:1045–1048CrossRefPubMed Brunette DM, Kenner GS, Gould TRL (1983) Grooved titanium surfaces orient growth and migration of cells from human gingival explants. J Dent Res 62:1045–1048CrossRefPubMed
68.
Zurück zum Zitat Martino MM, Tortelli F, Mochizuki M, Traub S, Ben-David D, Kuhn GA, Müller R, Livne E, Eming SA, Hubbell JA (2011) Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci Transl Med 3:100ra89PubMed Martino MM, Tortelli F, Mochizuki M, Traub S, Ben-David D, Kuhn GA, Müller R, Livne E, Eming SA, Hubbell JA (2011) Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci Transl Med 3:100ra89PubMed
69.
Zurück zum Zitat Aspriello SD, Zizzi A, Spazzafumo L, Rubini C, Lorenzi T, Marzioni D, Bullon P, Piemontese M (2011) Effects of enamel matrix derivative on vascular endothelial growth factor expression and microvessel density in gingival tissues of periodontal pocket: a comparative study. J Periodontol 82:606–612. doi:10.1902/jop.2010.100180 CrossRefPubMed Aspriello SD, Zizzi A, Spazzafumo L, Rubini C, Lorenzi T, Marzioni D, Bullon P, Piemontese M (2011) Effects of enamel matrix derivative on vascular endothelial growth factor expression and microvessel density in gingival tissues of periodontal pocket: a comparative study. J Periodontol 82:606–612. doi:10.​1902/​jop.​2010.​100180 CrossRefPubMed
72.
Zurück zum Zitat Spahr A, Lyngstadaas SP, Boeckh C, Andersson C, Podbielski A, Haller B (2002) Effect of the enamel matrix derivative Emdogain on the growth of periodontal pathogens in vitro. J Clin Periodontol 29:62–72CrossRefPubMed Spahr A, Lyngstadaas SP, Boeckh C, Andersson C, Podbielski A, Haller B (2002) Effect of the enamel matrix derivative Emdogain on the growth of periodontal pathogens in vitro. J Clin Periodontol 29:62–72CrossRefPubMed
75.
Zurück zum Zitat Sculean A, Auschill TM, Donos N, Brecx M, Arweiler NB (2001) Effect of an enamel matrix protein derivative (Emdogain) on ex vivo dental plaque vitality. J Clin Periodontol 28:1074–1078CrossRefPubMed Sculean A, Auschill TM, Donos N, Brecx M, Arweiler NB (2001) Effect of an enamel matrix protein derivative (Emdogain) on ex vivo dental plaque vitality. J Clin Periodontol 28:1074–1078CrossRefPubMed
76.
Zurück zum Zitat Wang Y, Zhang Y and Miron RJ (2015) Health, maintenance, and recovery of soft tissues around implants. Clinical implant dentistry and related research. doi: 10.1111/cid.12343 Wang Y, Zhang Y and Miron RJ (2015) Health, maintenance, and recovery of soft tissues around implants. Clinical implant dentistry and related research. doi: 10.​1111/​cid.​12343
77.
Zurück zum Zitat Froum SJ, Froum SH, Rosen PS (2012) Successful management of peri-implantitis with a regenerative approach: a consecutive series of 51 treated implants with 3- to 7.5-year follow-up. International Journal of Periodontics and Restorative Dentistry 32:11PubMed Froum SJ, Froum SH, Rosen PS (2012) Successful management of peri-implantitis with a regenerative approach: a consecutive series of 51 treated implants with 3- to 7.5-year follow-up. International Journal of Periodontics and Restorative Dentistry 32:11PubMed
Metadaten
Titel
Enamel matrix derivative improves gingival fibroblast cell behavior cultured on titanium surfaces
verfasst von
Yulan Wang
Yufeng Zhang
Dai Jing
Yang Shuang
Richard J. Miron
Publikationsdatum
14.08.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 4/2016
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-015-1558-5

Weitere Artikel der Ausgabe 4/2016

Clinical Oral Investigations 4/2016 Zur Ausgabe

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.