Concentration- and time-dependent response of human gingival fibroblasts to fibroblast growth factor 2 immobilized on titanium dental implants
Identifieur interne : 001F29 ( Pmc/Checkpoint ); précédent : 001F28; suivant : 001F30Concentration- and time-dependent response of human gingival fibroblasts to fibroblast growth factor 2 immobilized on titanium dental implants
Auteurs : Qianli Ma [République populaire de Chine] ; Wei Wang [République populaire de Chine] ; Paul K. Chu [République populaire de Chine] ; Shenglin Mei [République populaire de Chine] ; Kun Ji [République populaire de Chine] ; Lei Jin [République populaire de Chine] ; Yumei Zhang [République populaire de Chine]Source :
- International Journal of Nanomedicine [ 1176-9114 ] ; 2012.
Abstract
Titanium (Ti) implants are widely used clinically, but peri-implantitis remains one of the most common and serious complications. Healthy integration between gingival tissue and the implant surface is critical to long-term success in dental implant therapy. The objective of this study was to investigate how different concentrations of immobilized fibroblast growth factor 2 (FGF2) on the titania nanotubular surface influence the response of human gingival fibroblasts (HGFs).
Pure Ti metal was anodized at 20 V to form a vertically organized titanium dioxide nanotube array on which three concentrations of FGF2 (250 ng/mL, 500 ng/mL, or 1000 ng/mL) were immobilized by repeated lyophilization. Surface topography was observed and FGF2 elution was detected using enzyme-linked immunosorbent assay. The bioactivity changes of dissolvable immobilized FGF2 were measured by methyl-thiazolyl-tetrazolium assay. Behavior of HGFs was evaluated using adhesion and methyl-thiazolyl-tetrazolium bromide assays.
The FGF2 remained for several days on the modified surface on which HGFs were cultured. Over 90% of the dissolvable immobilized FGF2 had been eluted by Day 9, whereas the FGF2 activity was found to diminish gradually from Day 1 to Day 9. The titania nanotubular surface with an optimal preparing concentration (500 ng/mL) of FGF2 immobilization exhibited improved HGF functions such as cellular attachment, proliferation, and extracellular matrix-related gene expression. Moreover, significant bidirectional as well as concentration- and time-dependent bioactivity was observed.
Synergism of the FGF2-impregnated titanium dioxide nanotubular surface revealed good gingival-implant integration, indicating that these materials might have promising applications in dentistry and other biomedical devices.
Url:
DOI: 10.2147/IJN.S29538
PubMed: 22619534
PubMed Central: 3356224
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Chu</name><affiliation wicri:level="1"><nlm:aff id="af2-ijn-7-1965">Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong</wicri:regionArea><wicri:noRegion>Hong Kong</wicri:noRegion></affiliation></author><author><name sortKey="Mei, Shenglin" sort="Mei, Shenglin" uniqKey="Mei S" first="Shenglin" last="Mei">Shenglin Mei</name><affiliation wicri:level="1"><nlm:aff id="af1-ijn-7-1965">Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-ijn-7-1965">Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong</wicri:regionArea><wicri:noRegion>Hong Kong</wicri:noRegion></affiliation></author><author><name sortKey="Ji, Kun" sort="Ji, Kun" uniqKey="Ji K" first="Kun" last="Ji">Kun Ji</name><affiliation wicri:level="1"><nlm:aff id="af3-ijn-7-1965">Department of Pediatric Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Pediatric Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation></author><author><name sortKey="Jin, Lei" sort="Jin, Lei" uniqKey="Jin L" first="Lei" last="Jin">Lei Jin</name><affiliation wicri:level="1"><nlm:aff id="af4-ijn-7-1965">Stomatology Department, Jinling Hospital, School of Medicine, Southern Medical University, Nanjing, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Stomatology Department, Jinling Hospital, School of Medicine, Southern Medical University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Yumei" sort="Zhang, Yumei" uniqKey="Zhang Y" first="Yumei" last="Zhang">Yumei Zhang</name><affiliation wicri:level="1"><nlm:aff id="af1-ijn-7-1965">Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22619534</idno><idno type="pmc">3356224</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3356224</idno><idno type="RBID">PMC:3356224</idno><idno type="doi">10.2147/IJN.S29538</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">002E49</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002E49</idno><idno type="wicri:Area/Pmc/Curation">002E49</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002E49</idno><idno type="wicri:Area/Pmc/Checkpoint">001F29</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">001F29</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Concentration- and time-dependent response of human gingival fibroblasts to fibroblast growth factor 2 immobilized on titanium dental implants</title><author><name sortKey="Ma, Qianli" sort="Ma, Qianli" uniqKey="Ma Q" first="Qianli" last="Ma">Qianli Ma</name><affiliation wicri:level="1"><nlm:aff id="af1-ijn-7-1965">Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name><affiliation wicri:level="1"><nlm:aff id="af1-ijn-7-1965">Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation></author><author><name sortKey="Chu, Paul K" sort="Chu, Paul K" uniqKey="Chu P" first="Paul K" last="Chu">Paul K. Chu</name><affiliation wicri:level="1"><nlm:aff id="af2-ijn-7-1965">Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong</wicri:regionArea><wicri:noRegion>Hong Kong</wicri:noRegion></affiliation></author><author><name sortKey="Mei, Shenglin" sort="Mei, Shenglin" uniqKey="Mei S" first="Shenglin" last="Mei">Shenglin Mei</name><affiliation wicri:level="1"><nlm:aff id="af1-ijn-7-1965">Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-ijn-7-1965">Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong</wicri:regionArea><wicri:noRegion>Hong Kong</wicri:noRegion></affiliation></author><author><name sortKey="Ji, Kun" sort="Ji, Kun" uniqKey="Ji K" first="Kun" last="Ji">Kun Ji</name><affiliation wicri:level="1"><nlm:aff id="af3-ijn-7-1965">Department of Pediatric Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Pediatric Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation></author><author><name sortKey="Jin, Lei" sort="Jin, Lei" uniqKey="Jin L" first="Lei" last="Jin">Lei Jin</name><affiliation wicri:level="1"><nlm:aff id="af4-ijn-7-1965">Stomatology Department, Jinling Hospital, School of Medicine, Southern Medical University, Nanjing, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Stomatology Department, Jinling Hospital, School of Medicine, Southern Medical University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Yumei" sort="Zhang, Yumei" uniqKey="Zhang Y" first="Yumei" last="Zhang">Yumei Zhang</name><affiliation wicri:level="1"><nlm:aff id="af1-ijn-7-1965">Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an</wicri:regionArea><wicri:noRegion>Xi’an</wicri:noRegion></affiliation></author></analytic><series><title level="j">International Journal of Nanomedicine</title><idno type="ISSN">1176-9114</idno><idno type="eISSN">1178-2013</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Titanium (Ti) implants are widely used clinically, but peri-implantitis remains one of the most common and serious complications. Healthy integration between gingival tissue and the implant surface is critical to long-term success in dental implant therapy. The objective of this study was to investigate how different concentrations of immobilized fibroblast growth factor 2 (FGF2) on the titania nanotubular surface influence the response of human gingival fibroblasts (HGFs).</p></sec><sec><title>Methods</title><p>Pure Ti metal was anodized at 20 V to form a vertically organized titanium dioxide nanotube array on which three concentrations of FGF2 (250 ng/mL, 500 ng/mL, or 1000 ng/mL) were immobilized by repeated lyophilization. Surface topography was observed and FGF2 elution was detected using enzyme-linked immunosorbent assay. The bioactivity changes of dissolvable immobilized FGF2 were measured by methyl-thiazolyl-tetrazolium assay. Behavior of HGFs was evaluated using adhesion and methyl-thiazolyl-tetrazolium bromide assays.</p></sec><sec><title>Results</title><p>The FGF2 remained for several days on the modified surface on which HGFs were cultured. Over 90% of the dissolvable immobilized FGF2 had been eluted by Day 9, whereas the FGF2 activity was found to diminish gradually from Day 1 to Day 9. The titania nanotubular surface with an optimal preparing concentration (500 ng/mL) of FGF2 immobilization exhibited improved HGF functions such as cellular attachment, proliferation, and extracellular matrix-related gene expression. Moreover, significant bidirectional as well as concentration- and time-dependent bioactivity was observed.</p></sec><sec><title>Conclusion</title><p>Synergism of the FGF2-impregnated titanium dioxide nanotubular surface revealed good gingival-implant integration, indicating that these materials might have promising applications in dentistry and other biomedical devices.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Adell, R" uniqKey="Adell R">R Adell</name></author><author><name sortKey="Eriksson, B" uniqKey="Eriksson B">B Eriksson</name></author><author><name sortKey="Lekholm, U" uniqKey="Lekholm U">U Lekholm</name></author><author><name sortKey="Branemark, Pi" uniqKey="Branemark P">PI Branemark</name></author><author><name sortKey="Jemt, T" uniqKey="Jemt T">T Jemt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Arvidson, K" uniqKey="Arvidson K">K Arvidson</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Nanomedicine</journal-id><journal-id journal-id-type="iso-abbrev">Int J Nanomedicine</journal-id><journal-title-group><journal-title>International Journal of Nanomedicine</journal-title></journal-title-group><issn pub-type="ppub">1176-9114</issn><issn pub-type="epub">1178-2013</issn><publisher><publisher-name>Dove Medical Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22619534</article-id><article-id pub-id-type="pmc">3356224</article-id><article-id pub-id-type="doi">10.2147/IJN.S29538</article-id><article-id pub-id-type="publisher-id">ijn-7-1965</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Research</subject></subj-group></article-categories><title-group><article-title>Concentration- and time-dependent response of human gingival fibroblasts to fibroblast growth factor 2 immobilized on titanium dental implants</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Ma</surname><given-names>Qianli</given-names></name><xref ref-type="aff" rid="af1-ijn-7-1965">1</xref><xref ref-type="author-notes" rid="fn1-ijn-7-1965">*</xref></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Wei</given-names></name><xref ref-type="aff" rid="af1-ijn-7-1965">1</xref><xref ref-type="author-notes" rid="fn1-ijn-7-1965">*</xref></contrib><contrib contrib-type="author"><name><surname>Chu</surname><given-names>Paul K</given-names></name><xref ref-type="aff" rid="af2-ijn-7-1965">2</xref></contrib><contrib contrib-type="author"><name><surname>Mei</surname><given-names>Shenglin</given-names></name><xref ref-type="aff" rid="af1-ijn-7-1965">1</xref><xref ref-type="aff" rid="af2-ijn-7-1965">2</xref></contrib><contrib contrib-type="author"><name><surname>Ji</surname><given-names>Kun</given-names></name><xref ref-type="aff" rid="af3-ijn-7-1965">3</xref></contrib><contrib contrib-type="author"><name><surname>Jin</surname><given-names>Lei</given-names></name><xref ref-type="aff" rid="af4-ijn-7-1965">4</xref><xref ref-type="corresp" rid="c1-ijn-7-1965"></xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Yumei</given-names></name><xref ref-type="aff" rid="af1-ijn-7-1965">1</xref><xref ref-type="corresp" rid="c1-ijn-7-1965"></xref></contrib></contrib-group><aff id="af1-ijn-7-1965"><label>1</label>Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</aff><aff id="af2-ijn-7-1965"><label>2</label>Department of Physics and Materials Science, City University of Hong Kong, Kowloon, Hong Kong, People’s Republic of China</aff><aff id="af3-ijn-7-1965"><label>3</label>Department of Pediatric Dentistry, School of Stomatology, Fourth Military Medical University, Xi’an, People’s Republic of China</aff><aff id="af4-ijn-7-1965"><label>4</label>Stomatology Department, Jinling Hospital, School of Medicine, Southern Medical University, Nanjing, People’s Republic of China</aff><author-notes><corresp id="c1-ijn-7-1965">Correspondence: Yumei Zhang, Department of Prosthetic Dentistry, School of Stomatology, Fourth Military Medical University, 17 West Chang Le Road, Xi’an 710032, People’s Republic of China, Tel +86 29 84776090, Fax +86 29 84776096, Email <email>wqtzym@fmmu.edu.cn</email>. Lei Jin, Stomatology Department, Jinling Hospital, School of Medicine, Southern Medical University, 305 East Zhongshan Road, Nanjing, 210002, People’s Republic of China, Tel +86 25 80861166, Fax +86 25 80861166, Email <email>jindentist@gmail.com</email></corresp><fn id="fn1-ijn-7-1965"><label>*</label><p>These authors contributed equally to this work</p></fn></author-notes><pub-date pub-type="collection"><year>2012</year></pub-date><pmc-comment>Dove Press titles changed from ppub to collections in 2009.
Fake ppub written to satisfy Coll Date Type=ppub</pmc-comment>
<pub-date pub-type="ppub"><year>2012</year></pub-date><pub-date pub-type="epub"><day>17</day><month>4</month><year>2012</year></pub-date><volume>7</volume><fpage>1965</fpage><lpage>1976</lpage><permissions><copyright-statement>© 2012 Ma et al, publisher and licensee Dove Medical Press Ltd.</copyright-statement><copyright-year>2012</copyright-year><license><license-p>This is an Open Access article which permits unrestricted noncommercial use, provided the original work is properly cited.</license-p></license></permissions><abstract><sec><title>Background</title><p>Titanium (Ti) implants are widely used clinically, but peri-implantitis remains one of the most common and serious complications. Healthy integration between gingival tissue and the implant surface is critical to long-term success in dental implant therapy. The objective of this study was to investigate how different concentrations of immobilized fibroblast growth factor 2 (FGF2) on the titania nanotubular surface influence the response of human gingival fibroblasts (HGFs).</p></sec><sec><title>Methods</title><p>Pure Ti metal was anodized at 20 V to form a vertically organized titanium dioxide nanotube array on which three concentrations of FGF2 (250 ng/mL, 500 ng/mL, or 1000 ng/mL) were immobilized by repeated lyophilization. Surface topography was observed and FGF2 elution was detected using enzyme-linked immunosorbent assay. The bioactivity changes of dissolvable immobilized FGF2 were measured by methyl-thiazolyl-tetrazolium assay. Behavior of HGFs was evaluated using adhesion and methyl-thiazolyl-tetrazolium bromide assays.</p></sec><sec><title>Results</title><p>The FGF2 remained for several days on the modified surface on which HGFs were cultured. Over 90% of the dissolvable immobilized FGF2 had been eluted by Day 9, whereas the FGF2 activity was found to diminish gradually from Day 1 to Day 9. The titania nanotubular surface with an optimal preparing concentration (500 ng/mL) of FGF2 immobilization exhibited improved HGF functions such as cellular attachment, proliferation, and extracellular matrix-related gene expression. Moreover, significant bidirectional as well as concentration- and time-dependent bioactivity was observed.</p></sec><sec><title>Conclusion</title><p>Synergism of the FGF2-impregnated titanium dioxide nanotubular surface revealed good gingival-implant integration, indicating that these materials might have promising applications in dentistry and other biomedical devices.</p></sec></abstract><kwd-group><kwd>dental implants</kwd><kwd>titanium dioxide nanotube</kwd><kwd>fibroblast growth factor 2</kwd><kwd>extracellular matrix</kwd><kwd>real-time polymerase chain reaction</kwd></kwd-group></article-meta></front><floats-group><fig id="f1-ijn-7-1965" position="float"><label>Figure 1</label><caption><p>Immobilized FGF2 compared with FGF2-free samples initially and after 9 days.</p><p><bold>Abbreviations:</bold> FGF2, fibroblast growth factor 2; NT, nanotube; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f1"></graphic></fig><fig id="f2-ijn-7-1965" position="float"><label>Figure 2</label><caption><p>Field emission scanning electron microscopy results. (<bold>A</bold>) NT surface showed an NT array structure; NT-F-H surface showed clumps of fibroblast growth factor 2 and that the typical NT surface was changed. (<bold>B</bold>) Profile of titania NT.</p><p><bold>Note:</bold> The length of NT was 588.85 ± 31.92 nm (mean value ± standard deviation).</p><p><bold>Abbreviations:</bold> NT, nanotube; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f2"></graphic></fig><fig id="f3-ijn-7-1965" position="float"><label>Figure 3</label><caption><p>Atomic force microscopy images of different surfaces: (<bold>A</bold>) PT, (<bold>B</bold>) NT, (<bold>C</bold>) NT-F-L, (<bold>D</bold>) NT-F-M, and (<bold>E</bold>) NT-F-H. PT showed a microgroove structure, and porous-like structures were observed in other groups.</p><p><bold>Abbreviations:</bold> NT, nanotube; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f3"></graphic></fig><fig id="f4-ijn-7-1965" position="float"><label>Figure 4</label><caption><p>Elution kinetics of various FGF2 immobilizations. FGF2 eluted rapidly within first 3 days and the elution velocity reduced with time. Approximately all dissolvable FGF2 eluted within 30 days.</p><p><bold>Abbreviations:</bold> FGF2, fibroblast growth factor 2; NT, nanotube.</p></caption><graphic xlink:href="ijn-7-1965f4"></graphic></fig><fig id="f5-ijn-7-1965" position="float"><label>Figure 5</label><caption><p>HGF adhesion. (<bold>A</bold>) HGFs attached to the substrates with 4′,6′-diamidino-2-phenylindole stain and (<bold>B</bold>) relative cell adhesion rate of attached HGFs. The NT and NT-F-H surfaces inhibited cell adhesion, whereas the NT-F-L and NT-F-M improved cell attachment.</p><p><bold>Notes:</bold><sup>#</sup>Higher than PT (<italic>P</italic> < 0.01), *lower than PT (<italic>P</italic> < 0.01), difference also exists between 1*, 2*, 1<sup>#</sup>, and 2<sup>#</sup> (<italic>P</italic> < 0.01).</p><p><bold>Abbreviations:</bold> HGF, human gingival fibroblast; NT, nanotube; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f5"></graphic></fig><fig id="f6-ijn-7-1965" position="float"><label>Figure 6</label><caption><p>Cell proliferation measured by the methyl-thiazolyl-tetrazolium assay. NT-F-L and NT-F-M showed the higher cell proliferation at each interval, whereas NT-F-H with overimmobilized FGF2 showed the lowest at the early stage (Days 1 and 3).</p><p><bold>Notes:</bold><sup>#</sup>Higher than PT (<italic>P</italic> < 0.01), *lower than PT (<italic>P</italic> < 0.01), significant difference exists between 1<sup>#</sup> and 2<sup>#</sup> (<italic>P</italic> < 0.01).</p><p><bold>Abbreviations:</bold> FGF2, fibroblast growth factor 2; NT, nanotube; OD, optical density; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f6"></graphic></fig><fig id="f7-ijn-7-1965" position="float"><label>Figure 7</label><caption><p>Morphology of HGFs: (<bold>A</bold>) PT, (<bold>B</bold>) NT, (<bold>C</bold>) NT-F-L, (<bold>D</bold>) NT-F-M, and (<bold>E</bold>) NT-F-H lacking sufficient prominences/pseudopods and not fusing together.</p><p><bold>Abbreviations:</bold> HGF, human gingival fibroblast; NT, nanotube; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f7"></graphic></fig><fig id="f8-ijn-7-1965" position="float"><label>Figure 8</label><caption><p>Extracellular matrix-related gene expressions by HGFs cultured on four different titanium surfaces at Days 3, 6, and 9: (<bold>A</bold>) <italic>VEGFA</italic>, (<bold>B</bold>) <italic>ITGB</italic>, (<bold>C</bold>) <italic>ICAM1</italic>, and (<bold>D</bold>) <italic>LAMA1</italic>. Inverse concentration-dependent effects of NT-F-H were observed at Day 3 on (<bold>C</bold>) and (<bold>D</bold>).</p><p><bold>Notes:</bold><sup>#</sup>Upregulated compared with PT (<italic>P</italic> < 0.01), *downregulated (<italic>P</italic> < 0.01), significant difference exists between 1*, 2*, 1<sup>#</sup>, and 2<sup>#</sup> (<italic>P</italic> < 0.01).</p><p><bold>Abbreviations:</bold> HGF, human gingival fibroblast; <italic>ICAM1</italic>, intercellular adhesion molecule 1; <italic>ITGB</italic>, β-integrin; <italic>LAMA1</italic>, laminin-1; NT, nanotube; PT, polished titanium; <italic>VEGFA,</italic> vascular endothelial growth factor A.</p></caption><graphic xlink:href="ijn-7-1965f8"></graphic></fig><fig id="f9-ijn-7-1965" position="float"><label>Figure 9</label><caption><p>Activity changes of dissolvable FGF2 (10 ng/mL): control (FGF2-free); newly prepared Dulbecco’s modified Eagle’s medium; and S1, S3, S6, and S9 (FGF2 in Dulbecco’s modified Eagle’s medium stored for 1 day, 3 days, 6 days, or 9 days, respectively). The activity of FGF2 reduced gradually in culture medium with time and dropped to less than 50% after 9 days (S9) compared with NP.</p><p><bold>Note:</bold><sup>#</sup>Higher than PT (<italic>P</italic> < 0.01), significant difference exists between 1<sup>#</sup>, 2<sup>#</sup>, and 3<sup>#</sup> (<italic>P</italic> < 0.01).</p><p><bold>Abbreviations:</bold> FGF2, fibroblast growth factor 2; NT, nanotube; OD, optical density; PT, polished titanium.</p></caption><graphic xlink:href="ijn-7-1965f9"></graphic></fig><fig id="f10-ijn-7-1965" position="float"><label>Figure 10</label><caption><p>Pattern of nanotube-based FGF2 control release system: (<bold>A</bold>) initial stage, (<bold>B</bold>) in culture medium, FGF2 is gradually released from the nanotubes.</p><p><bold>Abbreviation:</bold> FGF2, fibroblast growth factor 2.</p></caption><graphic xlink:href="ijn-7-1965f10"></graphic></fig><table-wrap id="t1-ijn-7-1965" position="float"><label>Table 1</label><caption><p>Target cDNA primer sequences used in quantitative polymerase chain reaction</p></caption><table frame="hsides" rules="groups"><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>VEGFA</italic></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Forward: 5′-GAGCCTTGCCTTGCTGCTCTAC-3′</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Reverse: 5′-CACCAGGTCTCGATTGGATG-3′</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> PCR product size: 148 bp</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>ITGB</italic></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Forward: 5′-TGTGTCAGACCTGCCTTGGTG-3′</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Reverse: 5′-AGGAACATTCCTGTGTGCATGTG-3′</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> PCR product size: 105 bp</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>ICAM1</italic></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Forward: TGAGCAATGTGCAAGAAGATAGC</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Reverse: CCCGTTCTGGAGTCCAGTACA</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> PCR product size: 105 bp</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>LAMA1</italic></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Forward: TGGTAACATTTGCCACCACGA</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Reverse: TTGCCTCCGATCAGCATGAC</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> PCR product size: 127 bp</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>GAPDH</italic> (housekeeping gene)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Forward: 5′-GCACCGTCAAGGCTGAGAAC-3′</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> Reverse: 5′-TGGTGAAGACGCCAGTGGA-3′</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> PCR product size: 138 bp</td></tr></tbody></table><table-wrap-foot><fn id="tfn1-ijn-7-1965"><p><bold>Abbreviations:</bold><italic>GAPDH</italic>, glyceraldehyde 3-phosphate dehydrogenase; <italic>ICAM1</italic>, intercellular adhesion molecule 1; <italic>ITGB</italic>, β-integrin; <italic>LAMA1</italic>, laminin-1; <italic>VEGFA,</italic> vascular endothelial growth factor A.</p></fn></table-wrap-foot></table-wrap><table-wrap id="t2-ijn-7-1965" position="float"><label>Table 2</label><caption><p>Measurement of surface roughness by atomic force microscopy</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="top" rowspan="1" colspan="1">Group</th><th align="left" valign="top" rowspan="1" colspan="1">R<sub>a</sub></th><th align="left" valign="top" rowspan="1" colspan="1">RMS</th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">PT</td><td align="center" valign="top" rowspan="1" colspan="1">32.60 ± 3.45 nm</td><td align="center" valign="top" rowspan="1" colspan="1">41.70 ± 3.96 nm</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT</td><td align="center" valign="top" rowspan="1" colspan="1">4.96 ± 0.50 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td><td align="center" valign="top" rowspan="1" colspan="1">6.23 ± 0.80 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT-F-L</td><td align="center" valign="top" rowspan="1" colspan="1">7.25 ± 0.97 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td><td align="center" valign="top" rowspan="1" colspan="1">9.14 ± 1.25 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT-F-M</td><td align="center" valign="top" rowspan="1" colspan="1">9.70 ± 1.85 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td><td align="center" valign="top" rowspan="1" colspan="1">11.80 ± 2.21 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT-F-H</td><td align="center" valign="top" rowspan="1" colspan="1">9.42 ± 1.99 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td><td align="center" valign="top" rowspan="1" colspan="1">11.79 ± 2.35 nm<xref ref-type="table-fn" rid="tfn3-ijn-7-1965">*</xref></td></tr></tbody></table><table-wrap-foot><fn id="tfn2-ijn-7-1965"><p><bold>Notes:</bold></p></fn><fn id="tfn3-ijn-7-1965"><label>*</label><p>Lower R<sub>a</sub> and RMS compared with PT (<italic>P</italic> < 0.01). Anodization significantly smoothed titanium surface, whereas surface roughness was barely affected by FGF2 immobilization.</p></fn><fn id="tfn4-ijn-7-1965"><p><bold>Abbreviations:</bold> FGF2, fibroblast growth factor 2; NT, nanotube; PT, polished titanium; R<sub>a</sub>, average roughness, RMS, root mean square roughness.</p></fn></table-wrap-foot></table-wrap><table-wrap id="t3-ijn-7-1965" position="float"><label>Table 3</label><caption><p>Elution of dissolvable FGF2 at different time intervals<xref ref-type="table-fn" rid="tfn6-ijn-7-1965">*</xref></p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="top" rowspan="1" colspan="1">Time interval</th><th colspan="2" align="left" valign="top" rowspan="1">NT-F-L</th><th colspan="2" align="left" valign="top" rowspan="1">NT-F-M</th><th colspan="2" align="left" valign="top" rowspan="1">NT-F-H</th></tr><tr><th align="left" valign="top" rowspan="1" colspan="1"></th><th colspan="2" align="left" valign="top" rowspan="1"><hr></hr></th><th colspan="2" align="left" valign="top" rowspan="1"><hr></hr></th><th colspan="2" align="left" valign="top" rowspan="1"><hr></hr></th></tr><tr><th align="left" valign="top" rowspan="1" colspan="1"></th><th align="left" valign="top" rowspan="1" colspan="1">Mass (ng)</th><th align="left" valign="top" rowspan="1" colspan="1">Percent (accumulative)</th><th align="left" valign="top" rowspan="1" colspan="1">Mass (ng)</th><th align="left" valign="top" rowspan="1" colspan="1">Percent (accumulative)</th><th align="left" valign="top" rowspan="1" colspan="1">Mass (ng)</th><th align="left" valign="top" rowspan="1" colspan="1">Percent (accumulative)</th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">D0~D1</td><td align="left" valign="top" rowspan="1" colspan="1">10</td><td align="left" valign="top" rowspan="1" colspan="1">36.76</td><td align="left" valign="top" rowspan="1" colspan="1">24</td><td align="left" valign="top" rowspan="1" colspan="1">36.70</td><td align="left" valign="top" rowspan="1" colspan="1">35.6</td><td align="left" valign="top" rowspan="1" colspan="1">41.59</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D1~D2</td><td align="left" valign="top" rowspan="1" colspan="1">6</td><td align="left" valign="top" rowspan="1" colspan="1">58.82</td><td align="left" valign="top" rowspan="1" colspan="1">14.1</td><td align="left" valign="top" rowspan="1" colspan="1">58.26</td><td align="left" valign="top" rowspan="1" colspan="1">16.5</td><td align="left" valign="top" rowspan="1" colspan="1">60.86</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D2~D3</td><td align="left" valign="top" rowspan="1" colspan="1">3</td><td align="left" valign="top" rowspan="1" colspan="1">69.85</td><td align="left" valign="top" rowspan="1" colspan="1">7.9</td><td align="left" valign="top" rowspan="1" colspan="1">70.34</td><td align="left" valign="top" rowspan="1" colspan="1">8.9</td><td align="left" valign="top" rowspan="1" colspan="1">71.26</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D3~D6</td><td align="left" valign="top" rowspan="1" colspan="1">4.5</td><td align="left" valign="top" rowspan="1" colspan="1">86.40</td><td align="left" valign="top" rowspan="1" colspan="1">11.5</td><td align="left" valign="top" rowspan="1" colspan="1">87.92</td><td align="left" valign="top" rowspan="1" colspan="1">15.5</td><td align="left" valign="top" rowspan="1" colspan="1">89.37</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D6~D9</td><td align="left" valign="top" rowspan="1" colspan="1">1.5</td><td align="left" valign="top" rowspan="1" colspan="1">91.91</td><td align="left" valign="top" rowspan="1" colspan="1">4.5</td><td align="left" valign="top" rowspan="1" colspan="1">94.80</td><td align="left" valign="top" rowspan="1" colspan="1">5.7</td><td align="left" valign="top" rowspan="1" colspan="1">96.03</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D9~D15</td><td align="left" valign="top" rowspan="1" colspan="1">1.4</td><td align="left" valign="top" rowspan="1" colspan="1">97.06</td><td align="left" valign="top" rowspan="1" colspan="1">2.3</td><td align="left" valign="top" rowspan="1" colspan="1">98.32</td><td align="left" valign="top" rowspan="1" colspan="1">2.1</td><td align="left" valign="top" rowspan="1" colspan="1">98.48</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D15~D21</td><td align="left" valign="top" rowspan="1" colspan="1">0.6</td><td align="left" valign="top" rowspan="1" colspan="1">99.26</td><td align="left" valign="top" rowspan="1" colspan="1">0.7</td><td align="left" valign="top" rowspan="1" colspan="1">99.39</td><td align="left" valign="top" rowspan="1" colspan="1">0.8</td><td align="left" valign="top" rowspan="1" colspan="1">99.42</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D21~D30</td><td align="left" valign="top" rowspan="1" colspan="1">0.2</td><td align="left" valign="top" rowspan="1" colspan="1">100.00</td><td align="left" valign="top" rowspan="1" colspan="1">0.4</td><td align="left" valign="top" rowspan="1" colspan="1">100.00</td><td align="left" valign="top" rowspan="1" colspan="1">0.5</td><td align="left" valign="top" rowspan="1" colspan="1">100.00</td></tr></tbody></table><table-wrap-foot><fn id="tfn5-ijn-7-1965"><p><bold>Notes:</bold></p></fn><fn id="tfn6-ijn-7-1965"><label>*</label><p>Average amounts and accumulative percent of eluted FGF2 at each time interval. FGF2 rapidly eluted within the first 3 days, followed by a gradual reduction in elution. Over 90% of the dissolvable immobilized FGF2 eluted within 9 days. After 21 days, additional elution was negligible.</p></fn><fn id="tfn7-ijn-7-1965"><p><bold>Abbreviations:</bold> FGF2, fibroblast growth factor 2; NT, nanotube; PT, polished titanium.</p></fn></table-wrap-foot></table-wrap><table-wrap id="t4-ijn-7-1965" position="float"><label>Table 4</label><caption><p>Summary of extracellular matrix-related gene expressions on Days 3, 6, and 9</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="top" rowspan="1" colspan="1"></th><th colspan="3" align="left" valign="top" rowspan="1"><italic>VEGFA</italic></th><th colspan="3" align="left" valign="top" rowspan="1"><italic>ITGB</italic></th><th colspan="3" align="left" valign="top" rowspan="1"><italic>ICAM1</italic></th><th colspan="3" align="left" valign="top" rowspan="1"><italic>LAMA1</italic></th></tr><tr><th align="left" valign="top" rowspan="1" colspan="1"></th><th colspan="3" align="left" valign="top" rowspan="1"><hr></hr></th><th colspan="3" align="left" valign="top" rowspan="1"><hr></hr></th><th colspan="3" align="left" valign="top" rowspan="1"><hr></hr></th><th colspan="3" align="left" valign="top" rowspan="1"><hr></hr></th></tr><tr><th align="left" valign="top" rowspan="1" colspan="1"></th><th align="left" valign="top" rowspan="1" colspan="1">D3</th><th align="left" valign="top" rowspan="1" colspan="1">D6</th><th align="left" valign="top" rowspan="1" colspan="1">D9</th><th align="left" valign="top" rowspan="1" colspan="1">D3</th><th align="left" valign="top" rowspan="1" colspan="1">D6</th><th align="left" valign="top" rowspan="1" colspan="1">D9</th><th align="left" valign="top" rowspan="1" colspan="1">D3</th><th align="left" valign="top" rowspan="1" colspan="1">D6</th><th align="left" valign="top" rowspan="1" colspan="1">D9</th><th align="left" valign="top" rowspan="1" colspan="1">D3</th><th align="left" valign="top" rowspan="1" colspan="1">D6</th><th align="left" valign="top" rowspan="1" colspan="1">D9</th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">NT</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">/</td><td align="left" valign="top" rowspan="1" colspan="1">/</td><td align="left" valign="top" rowspan="1" colspan="1">/</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">/</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT-F-L</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">/</td><td align="left" valign="top" rowspan="1" colspan="1">/</td><td align="left" valign="top" rowspan="1" colspan="1">/</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT-F-M</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+4</td><td align="left" valign="top" rowspan="1" colspan="1">+4</td><td align="left" valign="top" rowspan="1" colspan="1">+4</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">NT-F-H</td><td align="left" valign="top" rowspan="1" colspan="1">+4</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+3</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">−</td><td align="left" valign="top" rowspan="1" colspan="1">+2</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">−</td><td align="left" valign="top" rowspan="1" colspan="1">+</td><td align="left" valign="top" rowspan="1" colspan="1">+</td></tr></tbody></table><table-wrap-foot><fn id="tfn8-ijn-7-1965"><p><bold>Notes: +</bold>, Upregulated compared with PT (<italic>P</italic> < 0.01); −, downregulated (<italic>P</italic> < 0.01);<bold>/</bold>, no significant difference compared with PT.</p></fn><fn id="tfn9-ijn-7-1965"><p><bold>Abbreviations:</bold><italic>ICAM1</italic>, intercellular adhesion molecule 1; <italic>ITGB</italic>, β-integrin; <italic>LAMA1</italic>, laminin-1; NT, nanotube; PT, polished titanium; <italic>VEGFA,</italic> vascular endothelial growth factor A.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Ma, Qianli" sort="Ma, Qianli" uniqKey="Ma Q" first="Qianli" last="Ma">Qianli Ma</name></noRegion><name sortKey="Chu, Paul K" sort="Chu, Paul K" uniqKey="Chu P" first="Paul K" last="Chu">Paul K. Chu</name><name sortKey="Ji, Kun" sort="Ji, Kun" uniqKey="Ji K" first="Kun" last="Ji">Kun Ji</name><name sortKey="Jin, Lei" sort="Jin, Lei" uniqKey="Jin L" first="Lei" last="Jin">Lei Jin</name><name sortKey="Mei, Shenglin" sort="Mei, Shenglin" uniqKey="Mei S" first="Shenglin" last="Mei">Shenglin Mei</name><name sortKey="Mei, Shenglin" sort="Mei, Shenglin" uniqKey="Mei S" first="Shenglin" last="Mei">Shenglin Mei</name><name sortKey="Wang, Wei" sort="Wang, Wei" uniqKey="Wang W" first="Wei" last="Wang">Wei Wang</name><name sortKey="Zhang, Yumei" sort="Zhang, Yumei" uniqKey="Zhang Y" first="Yumei" last="Zhang">Yumei Zhang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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