Estrogen enhances the bone regeneration potential of periodontal ligament stem cells derived from osteoporotic rats and seeded on nano-hydroxyapatite/collagen/poly(L-lactide)
Identifieur interne : 006635 ( Ncbi/Merge ); précédent : 006634; suivant : 006636Estrogen enhances the bone regeneration potential of periodontal ligament stem cells derived from osteoporotic rats and seeded on nano-hydroxyapatite/collagen/poly(L-lactide)
Auteurs : Ling-Ling E [République populaire de Chine] ; Wen-Huan Xu [République populaire de Chine] ; Lin Feng [République populaire de Chine] ; Yi Liu [République populaire de Chine] ; Dong-Qing Cai [République populaire de Chine] ; Ning Wen [République populaire de Chine] ; Wen-Jie Zheng [République populaire de Chine]Source :
- International Journal of Molecular Medicine [ 1107-3756 ] ; 2016.
Abstract
This study investigated the effects of estrogen on the bone regeneration potential of periodontal ligament stem cells (PDLSCs) derived from osteoporotic rats and seeded on a collagen-based composite scaffold [nano-hydroxyapatite/collagen/poly(L-lactide) (nHAC/PLA)]. For this purpose, 48 healthy 3-month-old Sprague-Dawley female rats were divided into 2 groups as follows: the bilaterally ovariectomized (OVX) rats and sham-operated rats. The PDLSCs were isolated at 3 months after surgery (by which time postmenopausal osteoporosis had developed). The effects of estrogen on the characteristics of these cells seeded in a culture plate and of the cells seeded on nHAC/PLA were then investigated. The PDLSC + nHAC/PLA constructs were implanted subcutaneously into the backs of severe combined immunodeficient (SCID) mice for 12 weeks in order to examine the role of estrogen in the bone formation ability of PDLSCs derived from osteoporotic rats. The results from methyl thiazolyl tetrazolium (MTT) assay revealed that the proliferation of the cells derived from the rats in the OVX group was significantly higher than that of the cells derived from the rats in the sham-operated group at the stage of logarithmic growth. The staining intensity of alkaline phosphatase (ALP) and the mineralization of the cells derived from the rats in the OVX group was significantly weaker than that of the cells from the rats in the sham-operated group. When the PDLSCs were seeded on nHAC/PLA, ALP activity, osteocalcin (OCN) secretion, mineral formation and the mRNA expression levels of ALP, OCN, estrogen receptor (ER)α and ERβ in the cells derived from the rats in the OVX group were markedly decreased. Treatment with 17β-estradiol (E2) significantly weakened the proliferative ability of the cells derived from the OVX group rats, and enhanced their osteogenic differentiation ability and the mRNA expression levels of ALP, OCN, ERα and ERβ. When the constructs were implanted into the backs of SCID mice for 12 weeks, the results of histological analysis indicated that the constructs derived from the OVX group rats had a few newly formed bones and osteoids; however, a great number of newly formed bones and osteoids were present in the ones from the sham-operated group and the OVX + E2 group rats. Our findings further indicate that estrogen deficiency impairs the osteogenic differentiation potential of PDLSCs, and that ER plays an important role in the bone regeneration ability of PDLSCs. Estrogen enhances the bone regeneration potential of PDLSCs derived from osteoporotic rats and seeded on nHAC/PLA. This study may provide insight into the clinical management of periodontal bone tissue repair in postmenopausal women with the use of estrogen-mediated PDLSCs seeded on nHAC/PLA.
Url:
DOI: 10.3892/ijmm.2016.2559
PubMed: 27082697
PubMed Central: 4866970
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China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xu, Wen Huan" sort="Xu, Wen Huan" uniqKey="Xu W" first="Wen-Huan" last="Xu">Wen-Huan Xu</name><affiliation wicri:level="1"><nlm:aff id="af2-ijmm-37-06-1475">Scientific Research Department, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853, P.R. China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Scientific Research Department, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Feng, Lin" sort="Feng, Lin" uniqKey="Feng L" first="Lin" last="Feng">Lin Feng</name><affiliation wicri:level="1"><nlm:aff id="af1-ijmm-37-06-1475">Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853, P.R. China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Liu, Yi" sort="Liu, Yi" uniqKey="Liu Y" first="Yi" last="Liu">Yi Liu</name><affiliation wicri:level="1"><nlm:aff id="af1-ijmm-37-06-1475">Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853, P.R. China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Cai, Dong Qing" sort="Cai, Dong Qing" uniqKey="Cai D" first="Dong-Qing" last="Cai">Dong-Qing Cai</name><affiliation wicri:level="1"><nlm:aff id="af3-ijmm-37-06-1475">Department of Chemistry, Jinan University, Guangzhou, Guangdong 510632, P.R. China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Chemistry, Jinan University, Guangzhou, Guangdong 510632</wicri:regionArea><wicri:noRegion>Guangdong 510632</wicri:noRegion></affiliation></author><author><name sortKey="Wen, Ning" sort="Wen, Ning" uniqKey="Wen N" first="Ning" last="Wen">Ning Wen</name><affiliation wicri:level="1"><nlm:aff id="af1-ijmm-37-06-1475">Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853, P.R. China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zheng, Wen Jie" sort="Zheng, Wen Jie" uniqKey="Zheng W" first="Wen-Jie" last="Zheng">Wen-Jie Zheng</name><affiliation wicri:level="1"><nlm:aff id="af3-ijmm-37-06-1475">Department of Chemistry, Jinan University, Guangzhou, Guangdong 510632, P.R. China</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Department of Chemistry, Jinan University, Guangzhou, Guangdong 510632</wicri:regionArea><wicri:noRegion>Guangdong 510632</wicri:noRegion></affiliation></author></analytic><series><title level="j">International Journal of Molecular Medicine</title><idno type="ISSN">1107-3756</idno><idno type="eISSN">1791-244X</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>This study investigated the effects of estrogen on the bone regeneration potential of periodontal ligament stem cells (PDLSCs) derived from osteoporotic rats and seeded on a collagen-based composite scaffold [nano-hydroxyapatite/collagen/poly(L-lactide) (nHAC/PLA)]. For this purpose, 48 healthy 3-month-old Sprague-Dawley female rats were divided into 2 groups as follows: the bilaterally ovariectomized (OVX) rats and sham-operated rats. The PDLSCs were isolated at 3 months after surgery (by which time postmenopausal osteoporosis had developed). The effects of estrogen on the characteristics of these cells seeded in a culture plate and of the cells seeded on nHAC/PLA were then investigated. The PDLSC + nHAC/PLA constructs were implanted subcutaneously into the backs of severe combined immunodeficient (SCID) mice for 12 weeks in order to examine the role of estrogen in the bone formation ability of PDLSCs derived from osteoporotic rats. The results from methyl thiazolyl tetrazolium (MTT) assay revealed that the proliferation of the cells derived from the rats in the OVX group was significantly higher than that of the cells derived from the rats in the sham-operated group at the stage of logarithmic growth. The staining intensity of alkaline phosphatase (ALP) and the mineralization of the cells derived from the rats in the OVX group was significantly weaker than that of the cells from the rats in the sham-operated group. When the PDLSCs were seeded on nHAC/PLA, ALP activity, osteocalcin (OCN) secretion, mineral formation and the mRNA expression levels of ALP, OCN, estrogen receptor (ER)α and ERβ in the cells derived from the rats in the OVX group were markedly decreased. Treatment with 17β-estradiol (E2) significantly weakened the proliferative ability of the cells derived from the OVX group rats, and enhanced their osteogenic differentiation ability and the mRNA expression levels of ALP, OCN, ERα and ERβ. When the constructs were implanted into the backs of SCID mice for 12 weeks, the results of histological analysis indicated that the constructs derived from the OVX group rats had a few newly formed bones and osteoids; however, a great number of newly formed bones and osteoids were present in the ones from the sham-operated group and the OVX + E2 group rats. Our findings further indicate that estrogen deficiency impairs the osteogenic differentiation potential of PDLSCs, and that ER plays an important role in the bone regeneration ability of PDLSCs. Estrogen enhances the bone regeneration potential of PDLSCs derived from osteoporotic rats and seeded on nHAC/PLA. This study may provide insight into the clinical management of periodontal bone tissue repair in postmenopausal women with the use of estrogen-mediated PDLSCs seeded on nHAC/PLA.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bertonazzi, A" uniqKey="Bertonazzi A">A Bertonazzi</name></author><author><name sortKey="Nelson, B" uniqKey="Nelson B">B Nelson</name></author><author><name sortKey="Salvador, J" uniqKey="Salvador J">J Salvador</name></author><author><name sortKey="Umland, E" uniqKey="Umland E">E Umland</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Daniell, Hw" uniqKey="Daniell H">HW Daniell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tominari, T" uniqKey="Tominari T">T Tominari</name></author><author><name sortKey="Hirata, M" uniqKey="Hirata M">M Hirata</name></author><author><name sortKey="Matsumoto, C" uniqKey="Matsumoto C">C Matsumoto</name></author><author><name sortKey="Inada, M" uniqKey="Inada M">M Inada</name></author><author><name sortKey="Miyaura, C" uniqKey="Miyaura C">C Miyaura</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kobayashi, M" uniqKey="Kobayashi M">M Kobayashi</name></author><author><name sortKey="Matsumoto, C" uniqKey="Matsumoto C">C Matsumoto</name></author><author><name sortKey="Hirata, M" uniqKey="Hirata M">M Hirata</name></author><author><name sortKey="Tominari, T" uniqKey="Tominari T">T Tominari</name></author><author><name sortKey="Inada, M" uniqKey="Inada M">M Inada</name></author><author><name sortKey="Miyaura, C" uniqKey="Miyaura C">C Miyaura</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Marques, Mr" uniqKey="Marques M">MR Marques</name></author><author><name sortKey="Da Silva, Ma" uniqKey="Da Silva M">MA da Silva</name></author><author><name sortKey="Manzi, Fr" uniqKey="Manzi F">FR Manzi</name></author><author><name sortKey="Cesar Neto, Jb" uniqKey="Cesar Neto J">JB Cesar-Neto</name></author><author><name sortKey="Nociti, Fh" uniqKey="Nociti F">FH Nociti</name></author><author><name sortKey="Barros, Sp" uniqKey="Barros S">SP Barros</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Duarte, Pm" uniqKey="Duarte P">PM Duarte</name></author><author><name sortKey="De Assis, Dr" uniqKey="De Assis D">DR de Assis</name></author><author><name sortKey="Casati, Mz" uniqKey="Casati M">MZ Casati</name></author><author><name sortKey="Sallum, Aw" uniqKey="Sallum A">AW Sallum</name></author><author><name sortKey="Sallum, Ea" uniqKey="Sallum E">EA Sallum</name></author><author><name sortKey="Nociti, Fh" uniqKey="Nociti F">FH Nociti</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Reinhardt, Ra" uniqKey="Reinhardt R">RA Reinhardt</name></author><author><name sortKey="Payne, Jb" uniqKey="Payne J">JB Payne</name></author><author><name sortKey="Maze, Ca" uniqKey="Maze C">CA Maze</name></author><author><name sortKey="Patil, Kd" uniqKey="Patil K">KD Patil</name></author><author><name sortKey="Gallagher, Sj" uniqKey="Gallagher S">SJ Gallagher</name></author><author><name sortKey="Mattson, Js" uniqKey="Mattson J">JS Mattson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Palomo, L" uniqKey="Palomo L">L Palomo</name></author><author><name sortKey="Chitguppi, R" uniqKey="Chitguppi R">R Chitguppi</name></author><author><name sortKey="Buencamino, Mc" uniqKey="Buencamino M">MC Buencamino</name></author><author><name sortKey="Santos, D" uniqKey="Santos D">D Santos</name></author><author><name sortKey="Thacker, H" uniqKey="Thacker H">H Thacker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pepelassi, E" uniqKey="Pepelassi E">E Pepelassi</name></author><author><name sortKey="Nicopoulou Karayianni, K" uniqKey="Nicopoulou Karayianni K">K Nicopoulou-Karayianni</name></author><author><name sortKey="Archontopoulou, Ad" uniqKey="Archontopoulou A">AD Archontopoulou</name></author><author><name sortKey="Mitsea, A" uniqKey="Mitsea A">A Mitsea</name></author><author><name sortKey="Kavadella, A" uniqKey="Kavadella A">A Kavadella</name></author><author><name sortKey="Tsiklakis, K" uniqKey="Tsiklakis K">K Tsiklakis</name></author><author><name sortKey="Vrotsos, I" uniqKey="Vrotsos I">I Vrotsos</name></author><author><name sortKey="Devlin, H" uniqKey="Devlin H">H Devlin</name></author><author><name sortKey="Horner, K" uniqKey="Horner K">K Horner</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Haas, An" uniqKey="Haas A">AN Haas</name></author><author><name sortKey="Rosing, Ck" uniqKey="Rosing C">CK Rösing</name></author><author><name sortKey="Oppermann, Rv" uniqKey="Oppermann R">RV Oppermann</name></author><author><name sortKey="Albandar, Jm" uniqKey="Albandar J">JM Albandar</name></author><author><name sortKey="Susin, C" uniqKey="Susin C">C Susin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lerner, Uh" uniqKey="Lerner U">UH Lerner</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Taguchi, A" uniqKey="Taguchi A">A Taguchi</name></author><author><name sortKey="Tanimoto, K" uniqKey="Tanimoto K">K Tanimoto</name></author><author><name sortKey="Suei, Y" uniqKey="Suei Y">Y Suei</name></author><author><name sortKey="Otani, K" uniqKey="Otani K">K Otani</name></author><author><name sortKey="Wada, T" uniqKey="Wada T">T Wada</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Klemetti, E" uniqKey="Klemetti E">E Klemetti</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hirai, T" uniqKey="Hirai T">T Hirai</name></author><author><name sortKey="Ishijima, T" uniqKey="Ishijima T">T Ishijima</name></author><author><name sortKey="Hashikawa, Y" uniqKey="Hashikawa Y">Y Hashikawa</name></author><author><name sortKey="Yajima, T" uniqKey="Yajima T">T Yajima</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Von Wowern, N" uniqKey="Von Wowern N">N von Wowern</name></author><author><name sortKey="Kollerup, G" uniqKey="Kollerup G">G Kollerup</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Goncalves, Pf" uniqKey="Goncalves P">PF Gonçalves</name></author><author><name sortKey="Gurgel, Bc" uniqKey="Gurgel B">BC Gurgel</name></author><author><name sortKey="Pimentel, Sp" uniqKey="Pimentel S">SP Pimentel</name></author><author><name sortKey="Sallum, Ea" uniqKey="Sallum E">EA Sallum</name></author><author><name sortKey="Sallum, Aw" uniqKey="Sallum A">AW Sallum</name></author><author><name sortKey="Casati, Mz" uniqKey="Casati M">MZ Casati</name></author><author><name sortKey="Nociti, Fh" uniqKey="Nociti F">FH Nociti</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hoffmann, T" uniqKey="Hoffmann T">T Hoffmann</name></author><author><name sortKey="Richter, S" uniqKey="Richter S">S Richter</name></author><author><name sortKey="Meyle, J" uniqKey="Meyle J">J Meyle</name></author><author><name sortKey="Gonzales, Jr" uniqKey="Gonzales J">JR Gonzales</name></author><author><name sortKey="Heinz, B" uniqKey="Heinz B">B Heinz</name></author><author><name sortKey="Arjomand, M" uniqKey="Arjomand M">M Arjomand</name></author><author><name sortKey="Sculean, A" uniqKey="Sculean A">A Sculean</name></author><author><name sortKey="Reich, E" uniqKey="Reich E">E Reich</name></author><author><name sortKey="Jepsen, K" uniqKey="Jepsen K">K Jepsen</name></author><author><name sortKey="Jepsen, S" uniqKey="Jepsen S">S Jepsen</name></author><author><name sortKey="Boedeker, Rh" uniqKey="Boedeker R">RH Boedeker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Needleman, Ig" uniqKey="Needleman I">IG Needleman</name></author><author><name sortKey="Worthington, Hv" uniqKey="Worthington H">HV Worthington</name></author><author><name sortKey="Giedrys Leeper, E" uniqKey="Giedrys Leeper E">E Giedrys-Leeper</name></author><author><name sortKey="Tucker, Rj" uniqKey="Tucker R">RJ Tucker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Venezia, E" uniqKey="Venezia E">E Venezia</name></author><author><name sortKey="Goldstein, M" uniqKey="Goldstein M">M Goldstein</name></author><author><name sortKey="Boyan, Bd" uniqKey="Boyan B">BD Boyan</name></author><author><name sortKey="Schwartz, Z" uniqKey="Schwartz Z">Z Schwartz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kaigler, D" uniqKey="Kaigler D">D Kaigler</name></author><author><name sortKey="Cirelli, Ja" uniqKey="Cirelli J">JA Cirelli</name></author><author><name sortKey="Giannobile, Wv" uniqKey="Giannobile W">WV Giannobile</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Blumenthal, Nm" uniqKey="Blumenthal N">NM Blumenthal</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liu, Y" uniqKey="Liu Y">Y Liu</name></author><author><name sortKey="Zheng, Y" uniqKey="Zheng Y">Y Zheng</name></author><author><name sortKey="Ding, G" uniqKey="Ding G">G Ding</name></author><author><name sortKey="Fang, D" uniqKey="Fang D">D Fang</name></author><author><name sortKey="Zhang, C" uniqKey="Zhang C">C Zhang</name></author><author><name sortKey="Bartold, Pm" uniqKey="Bartold P">PM Bartold</name></author><author><name sortKey="Gronthos, S" uniqKey="Gronthos S">S Gronthos</name></author><author><name sortKey="Shi, S" uniqKey="Shi S">S Shi</name></author><author><name sortKey="Wang, S" uniqKey="Wang S">S Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Seo, Bm" uniqKey="Seo B">BM Seo</name></author><author><name sortKey="Miura, M" uniqKey="Miura M">M Miura</name></author><author><name sortKey="Gronthos, S" uniqKey="Gronthos S">S Gronthos</name></author><author><name sortKey="Bartold, Pm" uniqKey="Bartold P">PM Bartold</name></author><author><name sortKey="Batouli, S" uniqKey="Batouli S">S Batouli</name></author><author><name sortKey="Brahim, J" uniqKey="Brahim J">J Brahim</name></author><author><name sortKey="Young, M" uniqKey="Young M">M Young</name></author><author><name sortKey="Robey, Pg" uniqKey="Robey P">PG Robey</name></author><author><name sortKey="Wang, Cy" uniqKey="Wang C">CY Wang</name></author><author><name sortKey="Shi, S" uniqKey="Shi S">S Shi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhu, M" uniqKey="Zhu M">M Zhu</name></author><author><name sortKey="Kohan, E" uniqKey="Kohan E">E Kohan</name></author><author><name sortKey="Bradley, J" uniqKey="Bradley J">J Bradley</name></author><author><name sortKey="Hedrick, M" uniqKey="Hedrick M">M Hedrick</name></author><author><name sortKey="Benhaim, P" uniqKey="Benhaim P">P Benhaim</name></author><author><name sortKey="Zuk, P" uniqKey="Zuk P">P Zuk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aldahmash, A" uniqKey="Aldahmash A">A Aldahmash</name></author><author><name sortKey="Zaher, W" uniqKey="Zaher W">W Zaher</name></author><author><name sortKey="Al Nbaheen, M" uniqKey="Al Nbaheen M">M Al-Nbaheen</name></author><author><name sortKey="Kassem, M" uniqKey="Kassem M">M Kassem</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chen, Fp" uniqKey="Chen F">FP Chen</name></author><author><name sortKey="Hu, Ch" uniqKey="Hu C">CH Hu</name></author><author><name sortKey="Wang, Kc" uniqKey="Wang K">KC Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Morishita, M" uniqKey="Morishita M">M Morishita</name></author><author><name sortKey="Yamamura, T" uniqKey="Yamamura T">T Yamamura</name></author><author><name sortKey="Bachchu, Ma" uniqKey="Bachchu M">MA Bachchu</name></author><author><name sortKey="Shimazu, A" uniqKey="Shimazu A">A Shimazu</name></author><author><name sortKey="Iwamoto, Y" uniqKey="Iwamoto Y">Y Iwamoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Morishita, M" uniqKey="Morishita M">M Morishita</name></author><author><name sortKey="Yamamura, T" uniqKey="Yamamura T">T Yamamura</name></author><author><name sortKey="Shimazu, A" uniqKey="Shimazu A">A Shimazu</name></author><author><name sortKey="Bachchu, Ah" uniqKey="Bachchu A">AH Bachchu</name></author><author><name sortKey="Iwamoto, Y" uniqKey="Iwamoto Y">Y Iwamoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mamalis, A" uniqKey="Mamalis A">A Mamalis</name></author><author><name sortKey="Markopoulou, C" uniqKey="Markopoulou C">C Markopoulou</name></author><author><name sortKey="Lagou, A" uniqKey="Lagou A">A Lagou</name></author><author><name sortKey="Vrotsos, I" uniqKey="Vrotsos I">I Vrotsos</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liang, L" uniqKey="Liang L">L Liang</name></author><author><name sortKey="Yu, Jf" uniqKey="Yu J">JF Yu</name></author><author><name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name></author><author><name sortKey="Wang, G" uniqKey="Wang G">G Wang</name></author><author><name sortKey="Ding, Y" uniqKey="Ding Y">Y Ding</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cao, M" uniqKey="Cao M">M Cao</name></author><author><name sortKey="Shu, L" uniqKey="Shu L">L Shu</name></author><author><name sortKey="Li, J" uniqKey="Li J">J Li</name></author><author><name sortKey="Su, J" uniqKey="Su J">J Su</name></author><author><name sortKey="Zhang, W" uniqKey="Zhang W">W Zhang</name></author><author><name sortKey="Wang, Q" uniqKey="Wang Q">Q Wang</name></author><author><name sortKey="Guo, T" uniqKey="Guo T">T Guo</name></author><author><name sortKey="Ding, Y" uniqKey="Ding Y">Y Ding</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhang, B" uniqKey="Zhang B">B Zhang</name></author><author><name sortKey="Li, Y" uniqKey="Li Y">Y Li</name></author><author><name sortKey="Zhou, Q" uniqKey="Zhou Q">Q Zhou</name></author><author><name sortKey="Ding, Y" uniqKey="Ding Y">Y Ding</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liao, S" uniqKey="Liao S">S Liao</name></author><author><name sortKey="Wang, W" uniqKey="Wang W">W Wang</name></author><author><name sortKey="Uo, M" uniqKey="Uo M">M Uo</name></author><author><name sortKey="Ohkawa, S" uniqKey="Ohkawa S">S Ohkawa</name></author><author><name sortKey="Akasaka, T" uniqKey="Akasaka T">T Akasaka</name></author><author><name sortKey="Tamura, K" uniqKey="Tamura K">K Tamura</name></author><author><name sortKey="Cui, F" uniqKey="Cui F">F Cui</name></author><author><name sortKey="Watari, F" uniqKey="Watari F">F Watari</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liu, Hc" uniqKey="Liu H">HC Liu</name></author><author><name sortKey="E, Ll" uniqKey="E L">LL e</name></author><author><name sortKey="Wang, Ds" uniqKey="Wang D">DS Wang</name></author><author><name sortKey="Su, F" uniqKey="Su F">F Su</name></author><author><name sortKey="Wu, X" uniqKey="Wu X">X Wu</name></author><author><name sortKey="Shi, Zp" uniqKey="Shi Z">ZP Shi</name></author><author><name sortKey="Lv, Y" uniqKey="Lv Y">Y Lv</name></author><author><name sortKey="Wang, Jz" uniqKey="Wang J">JZ Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yu, Sj" uniqKey="Yu S">SJ Yu</name></author><author><name sortKey="Liu, Hc" uniqKey="Liu H">HC Liu</name></author><author><name sortKey="Ling Ling, E" uniqKey="Ling Ling E">E Ling-Ling</name></author><author><name sortKey="Wang, Ds" uniqKey="Wang D">DS Wang</name></author><author><name sortKey="Zhu, Gx" uniqKey="Zhu G">GX Zhu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gay, Ic" uniqKey="Gay I">IC Gay</name></author><author><name sortKey="Chen, S" uniqKey="Chen S">S Chen</name></author><author><name sortKey="Macdougall, M" uniqKey="Macdougall M">M MacDougall</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zheng, W" uniqKey="Zheng W">W Zheng</name></author><author><name sortKey="Wang, S" uniqKey="Wang S">S Wang</name></author><author><name sortKey="Ma, D" uniqKey="Ma D">D Ma</name></author><author><name sortKey="Tang, L" uniqKey="Tang L">L Tang</name></author><author><name sortKey="Duan, Y" uniqKey="Duan Y">Y Duan</name></author><author><name sortKey="Jin, Y" uniqKey="Jin Y">Y Jin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="E, Ll" uniqKey="E L">LL E</name></author><author><name sortKey="Xu, Ll" uniqKey="Xu L">LL Xu</name></author><author><name sortKey="Wu, X" uniqKey="Wu X">X Wu</name></author><author><name sortKey="Wang, Ds" uniqKey="Wang D">DS Wang</name></author><author><name sortKey="Lv, Y" uniqKey="Lv Y">Y Lv</name></author><author><name sortKey="Wang, Jz" uniqKey="Wang J">JZ Wang</name></author><author><name sortKey="Liu, Hc" uniqKey="Liu H">HC Liu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Barrilleaux, B" uniqKey="Barrilleaux B">B Barrilleaux</name></author><author><name sortKey="Phinney, Dg" uniqKey="Phinney D">DG Phinney</name></author><author><name sortKey="Prockop, Dj" uniqKey="Prockop D">DJ Prockop</name></author><author><name sortKey="O Connor, Kc" uniqKey="O Connor K">KC O'Connor</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Caplan, Ai" uniqKey="Caplan A">AI Caplan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Eberli, D" uniqKey="Eberli D">D Eberli</name></author><author><name sortKey="Atala, A" uniqKey="Atala A">A Atala</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chang, Pc" uniqKey="Chang P">PC Chang</name></author><author><name sortKey="Chien, Ly" uniqKey="Chien L">LY Chien</name></author><author><name sortKey="Chong, Ly" uniqKey="Chong L">LY Chong</name></author><author><name sortKey="Kuo, Yp" uniqKey="Kuo Y">YP Kuo</name></author><author><name sortKey="Hsiao, Jk" uniqKey="Hsiao J">JK Hsiao</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fan, Jz" uniqKey="Fan J">JZ Fan</name></author><author><name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name></author><author><name sortKey="Meng, Y" uniqKey="Meng Y">Y Meng</name></author><author><name sortKey="Li, Gw" uniqKey="Li G">GW Li</name></author><author><name sortKey="Chang, Sx" uniqKey="Chang S">SX Chang</name></author><author><name sortKey="Nian, H" uniqKey="Nian H">H Nian</name></author><author><name sortKey="Liang, Yj" uniqKey="Liang Y">YJ Liang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lee, Jh" uniqKey="Lee J">JH Lee</name></author><author><name sortKey="Baek, Hr" uniqKey="Baek H">HR Baek</name></author><author><name sortKey="Lee, Km" uniqKey="Lee K">KM Lee</name></author><author><name sortKey="Zheng, Gb" uniqKey="Zheng G">GB Zheng</name></author><author><name sortKey="Shin, Sj" uniqKey="Shin S">SJ Shin</name></author><author><name sortKey="Shim, Hj" uniqKey="Shim H">HJ Shim</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fang, J" uniqKey="Fang J">J Fang</name></author><author><name sortKey="Yang, L" uniqKey="Yang L">L Yang</name></author><author><name sortKey="Zhang, R" uniqKey="Zhang R">R Zhang</name></author><author><name sortKey="Zhu, X" uniqKey="Zhu X">X Zhu</name></author><author><name sortKey="Wang, P" uniqKey="Wang P">P Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liu, Y" uniqKey="Liu Y">Y Liu</name></author><author><name sortKey="Wang, L" uniqKey="Wang L">L Wang</name></author><author><name sortKey="Liu, S" uniqKey="Liu S">S Liu</name></author><author><name sortKey="Liu, D" uniqKey="Liu D">D Liu</name></author><author><name sortKey="Chen, C" uniqKey="Chen C">C Chen</name></author><author><name sortKey="Xu, X" uniqKey="Xu X">X Xu</name></author><author><name sortKey="Chen, X" uniqKey="Chen X">X Chen</name></author><author><name sortKey="Shi, S" uniqKey="Shi S">S Shi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bressan, E" uniqKey="Bressan E">E Bressan</name></author><author><name sortKey="Ferroni, L" uniqKey="Ferroni L">L Ferroni</name></author><author><name sortKey="Gardin, C" uniqKey="Gardin C">C Gardin</name></author><author><name sortKey="Pinton, P" uniqKey="Pinton P">P Pinton</name></author><author><name sortKey="Stellini, E" uniqKey="Stellini E">E Stellini</name></author><author><name sortKey="Botticelli, D" uniqKey="Botticelli D">D Botticelli</name></author><author><name sortKey="Sivolella, S" uniqKey="Sivolella S">S Sivolella</name></author><author><name sortKey="Zavan, B" uniqKey="Zavan B">B Zavan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sato, C" uniqKey="Sato C">C Sato</name></author><author><name sortKey="Iso, Y" uniqKey="Iso Y">Y Iso</name></author><author><name sortKey="Mizukami, T" uniqKey="Mizukami T">T Mizukami</name></author><author><name sortKey="Otabe, K" uniqKey="Otabe K">K Otabe</name></author><author><name sortKey="Sasai, M" uniqKey="Sasai M">M Sasai</name></author><author><name sortKey="Kurata, M" uniqKey="Kurata M">M Kurata</name></author><author><name sortKey="Sanbe, T" uniqKey="Sanbe T">T Sanbe</name></author><author><name sortKey="Sekiya, I" uniqKey="Sekiya I">I Sekiya</name></author><author><name sortKey="Miyazaki, A" uniqKey="Miyazaki A">A Miyazaki</name></author><author><name sortKey="Suzuki, H" uniqKey="Suzuki H">H Suzuki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hong, Cj" uniqKey="Hong C">CJ Hong</name></author><author><name sortKey="Park, H" uniqKey="Park H">H Park</name></author><author><name sortKey="Yu, Sw" uniqKey="Yu S">SW Yu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Takashima, Y" uniqKey="Takashima Y">Y Takashima</name></author><author><name sortKey="Terada, M" uniqKey="Terada M">M Terada</name></author><author><name sortKey="Udono, M" uniqKey="Udono M">M Udono</name></author><author><name sortKey="Miura, S" uniqKey="Miura S">S Miura</name></author><author><name sortKey="Yamamoto, J" uniqKey="Yamamoto J">J Yamamoto</name></author><author><name sortKey="Suzuki, A" uniqKey="Suzuki A">A Suzuki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Larijani, B" uniqKey="Larijani B">B Larijani</name></author><author><name sortKey="Arjmand, B" uniqKey="Arjmand B">B Arjmand</name></author><author><name sortKey="Ahmadbeigi, N" uniqKey="Ahmadbeigi N">N Ahmadbeigi</name></author><author><name sortKey="Falahzadeh, K" uniqKey="Falahzadeh K">K Falahzadeh</name></author><author><name sortKey="Soleimani, M" uniqKey="Soleimani M">M Soleimani</name></author><author><name sortKey="Sayahpour, Fa" uniqKey="Sayahpour F">FA Sayahpour</name></author><author><name sortKey="Aghayan, Hr" uniqKey="Aghayan H">HR Aghayan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tong, L" uniqKey="Tong L">L Tong</name></author><author><name sortKey="Zhou, J" uniqKey="Zhou J">J Zhou</name></author><author><name sortKey="Rong, L" uniqKey="Rong L">L Rong</name></author><author><name sortKey="Seeley, Ej" uniqKey="Seeley E">EJ Seeley</name></author><author><name sortKey="Pan, J" uniqKey="Pan J">J Pan</name></author><author><name sortKey="Zhu, X" uniqKey="Zhu X">X Zhu</name></author><author><name sortKey="Liu, J" uniqKey="Liu J">J Liu</name></author><author><name sortKey="Wang, Q" uniqKey="Wang Q">Q Wang</name></author><author><name sortKey="Tang, X" uniqKey="Tang X">X Tang</name></author><author><name sortKey="Qu, J" uniqKey="Qu J">J Qu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Drowley, L" uniqKey="Drowley L">L Drowley</name></author><author><name sortKey="Koonce, C" uniqKey="Koonce C">C Koonce</name></author><author><name sortKey="Peel, S" uniqKey="Peel S">S Peel</name></author><author><name sortKey="Jonebring, A" uniqKey="Jonebring A">A Jonebring</name></author><author><name sortKey="Plowright, At" uniqKey="Plowright A">AT Plowright</name></author><author><name sortKey="Kattman, Sj" uniqKey="Kattman S">SJ Kattman</name></author><author><name sortKey="Andersson, H" uniqKey="Andersson H">H Andersson</name></author><author><name sortKey="Anson, B" uniqKey="Anson B">B Anson</name></author><author><name sortKey="Swanson, Bj" uniqKey="Swanson B">BJ Swanson</name></author><author><name sortKey="Wang, Qd" uniqKey="Wang Q">QD Wang</name></author><author><name sortKey="Brolen, G" uniqKey="Brolen G">G Brolen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tuganbekova, S" uniqKey="Tuganbekova S">S Tuganbekova</name></author><author><name sortKey="Gaipov, A" uniqKey="Gaipov A">A Gaipov</name></author><author><name sortKey="Turebekov, Z" uniqKey="Turebekov Z">Z Turebekov</name></author><author><name sortKey="Saparbayev, S" uniqKey="Saparbayev S">S Saparbayev</name></author><author><name sortKey="Shaimardanova, G" uniqKey="Shaimardanova G">G Shaimardanova</name></author><author><name sortKey="Popova, N" uniqKey="Popova N">N Popova</name></author><author><name sortKey="Taubaldiyeva, Z" uniqKey="Taubaldiyeva Z">Z Taubaldiyeva</name></author><author><name sortKey="Serebrennikova, D" uniqKey="Serebrennikova D">D Serebrennikova</name></author><author><name sortKey="Trimova, R" uniqKey="Trimova R">R Trimova</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Mol Med</journal-id><journal-id journal-id-type="iso-abbrev">Int. J. Mol. Med</journal-id><journal-id journal-id-type="publisher-id">IJMM</journal-id><journal-title-group><journal-title>International Journal of Molecular Medicine</journal-title></journal-title-group><issn pub-type="ppub">1107-3756</issn><issn pub-type="epub">1791-244X</issn><publisher><publisher-name>D.A. Spandidos</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27082697</article-id><article-id pub-id-type="pmc">4866970</article-id><article-id pub-id-type="doi">10.3892/ijmm.2016.2559</article-id><article-id pub-id-type="publisher-id">ijmm-37-06-1475</article-id><article-categories><subj-group subj-group-type="heading"><subject>Articles</subject></subj-group></article-categories><title-group><article-title>Estrogen enhances the bone regeneration potential of periodontal ligament stem cells derived from osteoporotic rats and seeded on nano-hydroxyapatite/collagen/poly(L-lactide)</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>E</surname><given-names>LING-LING</given-names></name><xref ref-type="aff" rid="af1-ijmm-37-06-1475">1</xref><xref rid="fn1-ijmm-37-06-1475" ref-type="author-notes">*</xref></contrib><contrib contrib-type="author"><name><surname>XU</surname><given-names>WEN-HUAN</given-names></name><xref ref-type="aff" rid="af2-ijmm-37-06-1475">2</xref><xref rid="fn1-ijmm-37-06-1475" ref-type="author-notes">*</xref></contrib><contrib contrib-type="author"><name><surname>FENG</surname><given-names>LIN</given-names></name><xref ref-type="aff" rid="af1-ijmm-37-06-1475">1</xref></contrib><contrib contrib-type="author"><name><surname>LIU</surname><given-names>YI</given-names></name><xref ref-type="aff" rid="af1-ijmm-37-06-1475">1</xref></contrib><contrib contrib-type="author"><name><surname>CAI</surname><given-names>DONG-QING</given-names></name><xref ref-type="aff" rid="af3-ijmm-37-06-1475">3</xref></contrib><contrib contrib-type="author"><name><surname>WEN</surname><given-names>NING</given-names></name><xref ref-type="aff" rid="af1-ijmm-37-06-1475">1</xref><xref ref-type="corresp" rid="c1-ijmm-37-06-1475"></xref></contrib><contrib contrib-type="author"><name><surname>ZHENG</surname><given-names>WEN-JIE</given-names></name><xref ref-type="aff" rid="af3-ijmm-37-06-1475">3</xref><xref ref-type="corresp" rid="c2-ijmm-37-06-1475"></xref></contrib></contrib-group><aff id="af1-ijmm-37-06-1475"><label>1</label>Institute of Stomatology, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853, P.R. China</aff><aff id="af2-ijmm-37-06-1475"><label>2</label>Scientific Research Department, Medical Administrative Division, Chinese PLA General Hospital, Beijing 100853, P.R. China</aff><aff id="af3-ijmm-37-06-1475"><label>3</label>Department of Chemistry, Jinan University, Guangzhou, Guangdong 510632, P.R. China</aff><author-notes><corresp id="c1-ijmm-37-06-1475">Correspondence to: Dr Ning Wen, Institute of Stomatology, Chinese PLA General Hospital, 28 Fuxing Road, Beijing 100853, P.R. China, E-mail: <email>wenningchn@163.com</email></corresp><corresp id="c2-ijmm-37-06-1475">Dr Wenjie Zheng, Department of Chemistry, Jinan University, 601 Huangpu Avenue West, Guangzhou, Guangdong 510632, P.R. China, E-mail: <email>tzhwj@jnu.cn</email></corresp><fn id="fn1-ijmm-37-06-1475"><label>*</label><p>Contributed equally</p></fn></author-notes><pub-date pub-type="ppub"><month>6</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>12</day><month>4</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>12</day><month>4</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>37</volume><issue>6</issue><fpage>1475</fpage><lpage>1486</lpage><history><date date-type="received"><day>21</day><month>7</month><year>2015</year></date><date date-type="accepted"><day>28</day><month>3</month><year>2016</year></date></history><permissions><copyright-statement>Copyright: © E et al.</copyright-statement><copyright-year>2016</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by-nc-nd/4.0/">Creative Commons Attribution-NonCommercial-NoDerivs License</ext-link>, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.</license-p></license></permissions><abstract><p>This study investigated the effects of estrogen on the bone regeneration potential of periodontal ligament stem cells (PDLSCs) derived from osteoporotic rats and seeded on a collagen-based composite scaffold [nano-hydroxyapatite/collagen/poly(L-lactide) (nHAC/PLA)]. For this purpose, 48 healthy 3-month-old Sprague-Dawley female rats were divided into 2 groups as follows: the bilaterally ovariectomized (OVX) rats and sham-operated rats. The PDLSCs were isolated at 3 months after surgery (by which time postmenopausal osteoporosis had developed). The effects of estrogen on the characteristics of these cells seeded in a culture plate and of the cells seeded on nHAC/PLA were then investigated. The PDLSC + nHAC/PLA constructs were implanted subcutaneously into the backs of severe combined immunodeficient (SCID) mice for 12 weeks in order to examine the role of estrogen in the bone formation ability of PDLSCs derived from osteoporotic rats. The results from methyl thiazolyl tetrazolium (MTT) assay revealed that the proliferation of the cells derived from the rats in the OVX group was significantly higher than that of the cells derived from the rats in the sham-operated group at the stage of logarithmic growth. The staining intensity of alkaline phosphatase (ALP) and the mineralization of the cells derived from the rats in the OVX group was significantly weaker than that of the cells from the rats in the sham-operated group. When the PDLSCs were seeded on nHAC/PLA, ALP activity, osteocalcin (OCN) secretion, mineral formation and the mRNA expression levels of ALP, OCN, estrogen receptor (ER)α and ERβ in the cells derived from the rats in the OVX group were markedly decreased. Treatment with 17β-estradiol (E2) significantly weakened the proliferative ability of the cells derived from the OVX group rats, and enhanced their osteogenic differentiation ability and the mRNA expression levels of ALP, OCN, ERα and ERβ. When the constructs were implanted into the backs of SCID mice for 12 weeks, the results of histological analysis indicated that the constructs derived from the OVX group rats had a few newly formed bones and osteoids; however, a great number of newly formed bones and osteoids were present in the ones from the sham-operated group and the OVX + E2 group rats. Our findings further indicate that estrogen deficiency impairs the osteogenic differentiation potential of PDLSCs, and that ER plays an important role in the bone regeneration ability of PDLSCs. Estrogen enhances the bone regeneration potential of PDLSCs derived from osteoporotic rats and seeded on nHAC/PLA. This study may provide insight into the clinical management of periodontal bone tissue repair in postmenopausal women with the use of estrogen-mediated PDLSCs seeded on nHAC/PLA.</p></abstract><kwd-group><kwd>periodontal diseases</kwd><kwd>postmenopausal osteoporosis</kwd><kwd>periodontal ligament stem cells</kwd><kwd>ovariectomy</kwd><kwd>estrogen</kwd><kwd>nano-hydroxyapatite/collagen/poly(L-lactide)</kwd></kwd-group></article-meta></front><floats-group><fig id="f1-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Effects of ovariectomy at 3 months after surgery on (A) body weight, (B) bone mineral density (BMD) and (C) estrogen level in the sham-operated (sham) and ovariectomized (OVX) group rats (n=24/group, means ± SD). <sup>*</sup>P<0.05, compared to sham group at the same time point.</p></caption><graphic xlink:href="IJMM-37-06-1475-g00"></graphic></fig><fig id="f2-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 2</label><caption><p>The periodontal ligament stem cells (PDLSCs) isolated from rats in the (A, C, E and G) sham-operated (sham) group and (B, D, F and H) ovariectomized (OVX) group expressed (C and D) STRO-1 and (E and G) vimentin, but did not express (F and H) keratin. (A and B) Magnification, ×200; (C and D) magnification, ×400; (E–H) magnification, ×600.</p></caption><graphic xlink:href="IJMM-37-06-1475-g01"></graphic></fig><fig id="f3-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Effect of estrogen on the proliferation of periodontal ligament stem cells (PDLSCs) isolated from rats in the ovariectomized (OVX) group over a period of 8 days (n=12 wells/plate, means ± SD). At the same time-point, <sup>*</sup>P<0.05, OVX vs. sham or OVX + E2; <sup>†</sup>P<0.05, OVX + E2 vs. sham; <sup>‡</sup>P<0.05, OVX + E2 vs. OVX. Sham, sham-operated group.</p></caption><graphic xlink:href="IJMM-37-06-1475-g02"></graphic></fig><fig id="f4-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Effect of estrogen on the osteogenic differentiation of periodontal ligament stem cells (PDLSCs). The cells from the (A and D) sham group, (B and E) OVX group and (C and F) OVX + E2 group were stained for (A–C) ALP and (D–F) mineralization. (A–C) Magnification, ×40; (D–F) magnification, ×100. OVX, ovariectomized; sham, sham-operated.</p></caption><graphic xlink:href="IJMM-37-06-1475-g03"></graphic></fig><fig id="f5-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 5</label><caption><p>Results from SEM showing the structure of (A) nHAC/PLA and the morphology of the cells in the (B) sham PDLSCs + nHAC/PLA, (C) OVX PDLSCs + nHAC/PLA and (D) OVX PDLSCs + nHAC/PLA + E2. (A) Magnification, ×400; (B–D) magnification, ×800. OVX, ovariectomized; PDLSCs, periodontal ligament stem cells; nHAC/PLA, nano-hydroxyapatite/collagen/poly(L-lactide).</p></caption><graphic xlink:href="IJMM-37-06-1475-g04"></graphic></fig><fig id="f6-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 6</label><caption><p>Effect of estrogen on (A) ALP activity and (B) osteocalcin secretion in OVX PDLSCs + nHAC/PLA (n=8 wells/plate, means ± SD). At same time period, <sup>*</sup>P<0.05, compared to OVX PDLSCs + nHAC/PLA; <sup>†</sup>P<0.05, compared to sham PDLSCs + nHAC/PLA. OVX, ovariectomized; PDLSCs, periodontal ligament stem cells; nHAC/PLA, nano-hydroxyapatite/collagen/poly(L-lactide).</p></caption><graphic xlink:href="IJMM-37-06-1475-g05"></graphic></fig><fig id="f7-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 7</label><caption><p>Effect of estrogen on (A) mineral formation and (B) ALP, (C) OCN, (D) ERα and (E) ERβ mRNA expression in OVX PDLSCs + nHAC/PLA (n=6 wells/plate, means ± SD). <sup>*</sup>P<0.05, compared to OVX PDLSCs + nHAC/PLA; <sup>†</sup>P<0.05, compared to sham PDLSCs + nHAC/PLA. OVX, ovariectomized; PDLSCs, periodontal ligament stem cells; nHAC/PLA, nano-hydroxyapatite/collagen/poly(L-lactide).</p></caption><graphic xlink:href="IJMM-37-06-1475-g06"></graphic></fig><fig id="f8-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 8</label><caption><p><italic>In vivo</italic> osteogenesis. (A) nHAC/PLA, (B) sham PDLSCs + nHAC/PLA, (C) OVX PDLSCs + nHAC/PLA, (D) OVX PDLSCs + nHAC/PLA + E2. Magnification, ×200, NB, newly formed bone. Black arrowheads indicate blood vessels, white arrowheads indicate osteoblastic cells. OVX, ovariectomized PDLSCs, periodontal ligament stem cells; nHAC/PLA, nano-hydroxyapatite/collagen/poly(L-lactide).</p></caption><graphic xlink:href="IJMM-37-06-1475-g07"></graphic></fig><fig id="f9-ijmm-37-06-1475" orientation="portrait" position="float"><label>Figure 9</label><caption><p>Percentage of bone formation area in each group after 12 weeks of implantation (n=6 constructs/group, mean ± SD). After 12 weeks, there were significant differences between all groups. Significance of the data at <sup>*</sup>P<0.05.</p></caption><graphic xlink:href="IJMM-37-06-1475-g08"></graphic></fig><table-wrap id="tI-ijmm-37-06-1475" orientation="portrait" position="float"><label>Table I</label><caption><p>Primers used for real-time PCR with SYBR-Green.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Gene</th><th valign="top" align="center" rowspan="1" colspan="1">Primer sequence</th><th valign="top" align="center" rowspan="1" colspan="1">Species</th><th valign="top" align="center" rowspan="1" colspan="1">Product size (bp)</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">ERα</td><td valign="top" align="left" rowspan="1" colspan="1">F: 5′-CAT CGA TAA GAA CCG GAG GA-3′</td><td valign="top" align="center" rowspan="1" colspan="1">Rat</td><td valign="top" align="center" rowspan="1" colspan="1">190</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">R: 5′-AAG GTT GGC AGC TCT CAT GT-3′</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">ERβ</td><td valign="top" align="left" rowspan="1" colspan="1">F: 5′-AGC AAC TGG TGC TCA CCC T-3′</td><td valign="top" align="center" rowspan="1" colspan="1">Rat</td><td valign="top" align="center" rowspan="1" colspan="1">94</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">R: 5′-GTC CGC CAG CTT AGT GAG G-3′</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">ALP</td><td valign="top" align="left" rowspan="1" colspan="1">F: 5′-TCC CAC GTT TTC ACG TTT-3′</td><td valign="top" align="center" rowspan="1" colspan="1">Rat</td><td valign="top" align="center" rowspan="1" colspan="1">140</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">R: 5′-GAG ACG TTC TCC CGT TCA C-3′</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">OCN</td><td valign="top" align="left" rowspan="1" colspan="1">F: 5′-TGA GGA CCC TCT CTC TGC TC-3</td><td valign="top" align="center" rowspan="1" colspan="1">Rat</td><td valign="top" align="center" rowspan="1" colspan="1">150</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">R: 5′-AGG TAGCGC CGG AGT CTA TT-3</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">β-actin</td><td valign="top" align="left" rowspan="1" colspan="1">F: 5′-CCC ATC TAT GAG GGT TAC GC-3′</td><td valign="top" align="center" rowspan="1" colspan="1">Rat</td><td valign="top" align="center" rowspan="1" colspan="1">150</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">R: 5′-TTT AAT GTC ACG CAC GAT TTC-3′</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td></tr></tbody></table><table-wrap-foot><fn id="tfn1-ijmm-37-06-1475"><p>F, forward; R, reverse; ER, estrogen receptor; OCN, osteocalcin.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li></country><settlement><li>Pékin</li></settlement></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="E, Ling Ling" sort="E, Ling Ling" uniqKey="E L" first="Ling-Ling" last="E">Ling-Ling E</name></noRegion><name sortKey="Cai, Dong Qing" sort="Cai, Dong Qing" uniqKey="Cai D" first="Dong-Qing" last="Cai">Dong-Qing Cai</name><name sortKey="Feng, Lin" sort="Feng, Lin" uniqKey="Feng L" first="Lin" last="Feng">Lin Feng</name><name sortKey="Liu, Yi" sort="Liu, Yi" uniqKey="Liu Y" first="Yi" last="Liu">Yi Liu</name><name sortKey="Wen, Ning" sort="Wen, Ning" uniqKey="Wen N" first="Ning" last="Wen">Ning Wen</name><name sortKey="Xu, Wen Huan" sort="Xu, Wen Huan" uniqKey="Xu W" first="Wen-Huan" last="Xu">Wen-Huan Xu</name><name sortKey="Zheng, Wen Jie" sort="Zheng, Wen Jie" uniqKey="Zheng W" first="Wen-Jie" last="Zheng">Wen-Jie Zheng</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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