Polyphenols from grape pomace induce osteogenic differentiation in mesenchymal stem cells
- Authors:
- Elisa Torre
- Giorgio Iviglia
- Clara Cassinelli
- Marco Morra
- Nazario Russo
-
Affiliations: Nobil Bio Ricerche srl, I‑14037 Portacomaro, Italy, University of Cagliari, I‑09124 Cagliari, Italy - Published online on: March 30, 2020 https://doi.org/10.3892/ijmm.2020.4556
- Pages: 1721-1734
-
Copyright: © Torre et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Palaska I, Papathanasiou E and Theoharides TC: Use of polyphenols in periodontal inflammation. Eur J Pharmacol. 720:77–83. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sankari SL, Babu NA, Rani V, Priyadharsini C and Masthan KM: Flavonoids-clinical effects and applications in dentistry: A review. J Pharm Bioallied Sci. 6(Suppl 1): S26–S29. 2014. View Article : Google Scholar : PubMed/NCBI | |
Bunte K, Hensel A and Beikler T: Polyphenols in the prevention and treatment of periodontal disease: A systematic review of in vivo, ex vivo and in vitro studies. Fitoterapia. 132:30–39. 2019. View Article : Google Scholar | |
Nazir MA: Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci (Qassim). 11:72–80. 2017. | |
Özden FO, Sakallioğlu EE, Sakallioğlu U, Ayas B and Erişgin Z: Effects of grape seed extract on periodontal disease: An experimental study in rats. J Appl Oral Sci. 25:121–129. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gennaro G, Claudino M, Cestari TM, Ceolin D, Germino P, Garlet GP and de Assis GF: Green tea modulates cytokine expression in the periodontium and attenuates alveolar bone resorption in type 1 diabetic rats. PLoS One. 10:e01347842015. View Article : Google Scholar : PubMed/NCBI | |
Tominari T, Hirata M, Matsumoto C, Inada M and Miyaura C: Polymethoxy flavonoids, nobiletin and tangeretin, prevent lipopolysaccharide-induced inflammatory bone loss in an experimental model for periodontitis. J Pharmacol Sci. 119:390–394. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fernández-Rojas B and Gutiérrez-Venegas G: Flavonoids exert multiple periodontic benefits including anti-inflammatory, periodontal ligament-supporting, and alveolar bone-preserving effects. Life Sci. 209:435–454. 2018. View Article : Google Scholar : PubMed/NCBI | |
Houde V, Grenier D and Chandad F: Protective effects of grape seed proanthocyanidins against oxidative stress induced by lipopolysaccharides of periodontopathogens. J Periodontol. 77:1371–1379. 2006. View Article : Google Scholar : PubMed/NCBI | |
Govindaraj J, Emmadi P, Deepalakshmi, Rajaram V, Prakash G and Puvanakrishnan R: Protective effect of proanthocyanidins on endotoxin induced experimental periodontitis in rats. Indian J Exp Biol. 48:133–142. 2010.PubMed/NCBI | |
Shen CL, Wang P, Guerrieri J, Yeh JK and Wang JS: Protective effect of green tea polyphenols on bone loss in middle-aged female rats. Osteoporos Int. 19:979–990. 2008. View Article : Google Scholar | |
Lee JH, Jin H, Shim HE, Kim HN, Ha H and Lee ZH: Epigallocatechin-3-gallate inhibits osteoclastogenesis by down-regulating c-Fos expression and suppressing the nuclear factor-kappaB signal. Mol Pharmacol. 77:17–25. 2010. View Article : Google Scholar | |
Nakamura H, Ukai T, Yoshimura A, Kozuka Y, Yoshioka H, Yoshinaga Y, Abe Y and Hara Y: Green tea catechin inhibits lipo-polysaccharide-induced bone resorption in vivo. J Periodontal Res. 45:23–30. 2010. View Article : Google Scholar | |
Gómez-Florit M, Monjo M and Ramis JM: Identification of quercitrin as potential therapeutic agent for periodontal applications. J Periodontol. 85:966–974. 2014. View Article : Google Scholar | |
Chen JR, Lazarenko OP, Wu X, Kang J, Blackburn ML, Shankar K, Badger TM and Ronis MJ: Dietary-induced serum phenolic acids promote bone growth via p38 MAPK/β-catenin canonical Wnt signaling. J Bone Miner Res. 25:2399–2411. 2010. View Article : Google Scholar : PubMed/NCBI | |
Bu SY, Hunt TS and Smith BJ: Dried plum polyphenols attenuate the detrimental effects of TNF-alpha on osteoblast function coincident with up-regulation of Runx2, Osterix and IGF-I. J Nutr Biochem. 20:35–44. 2009. View Article : Google Scholar | |
Trzeciakiewicz A, Habauzit V, Mercier S, Lebecque P, Davicco MJ, Coxam V, Demigne C and Horcajada MN: Hesperetin stimulates differentiation of primary rat osteoblasts involving the BMP signalling pathway. J Nutr Biochem. 21:424–431. 2010. View Article : Google Scholar | |
Byun MR, Sung MK, Kima AR, Lee CH, Jang EJ, Jeong MG, Noh M, Hwang ES and Hong JH: (-)-Epicatechin gallate (ECG) stimulates osteoblast differentiation via Runt-related transcription factor 2 (RUNX2) and transcriptional coactivator with PDZ-binding motif (TAZ)-mediated transcriptional activation. J Biol Chem. 289:9926–9935. 2014. View Article : Google Scholar : PubMed/NCBI | |
Santiago-Mora R, Casado-Díaz A, De Castro MD and Quesada-Gómez JM: Oleuropein enhances osteoblastogenesis and inhibits adipogenesis: The effect on differentiation in stem cells derived from bone marrow. Osteoporos Int. 22:675–684. 2011. View Article : Google Scholar | |
Patisaul HB and Jefferson W: The pros and cons of phytoestrogens. Front Neuroendocrinol. 31:400–419. 2010. View Article : Google Scholar : PubMed/NCBI | |
Torre E: Molecular signaling mechanisms behind polyphenol-induced bone anabolism. Phytochem Rev. 16:1183–1226. 2017. View Article : Google Scholar : PubMed/NCBI | |
Torre E, Iviglia G, Cassinelli C and Morra M: Potentials of poly-phenols in bone-implant devices. Polyphenols. Wong J: IntechOpen; 2018, https://www.intechopen.com/books/polyphe-nols/potentials-of-polyphenols-in-bone-implant-devices. Accessed April 11, 2018. View Article : Google Scholar | |
Sheikh Z, Sima C and Glogauer M: Bone replacement materials and techniques used for achieving vertical alveolar bone augmentation. Materials. 8:2953–2993. 2015. View Article : Google Scholar | |
Rodriguez Baena RY, Rizzo S, Manzo L and Lupi SM: Nanofeatured titanium surfaces for dental implantology: Biological effects, biocompatibility, and safety. J Nanomater. 2017:182017. View Article : Google Scholar | |
Morra M: Biomolecular modification of implant surfaces. Expert Rev Med Devices. 4:36–372. 2007. View Article : Google Scholar | |
Brett E, Flacco J, Blackshear C, Longaker MT and Wan DC: Biomimetics of bone implants: The regenerative road. Biores Open Access. 6:1–6. 2017. View Article : Google Scholar : PubMed/NCBI | |
Morra M, Cassinelli C, Torre E and Iviglia G: Permanent wettability of a novel, nanoengineered, clinically available, hyaluronan-coated dental implant. Clin Exp Dent Res. 4:196–205. 2018. View Article : Google Scholar : PubMed/NCBI | |
Bryers JD, Giachelli CM and Ratner BD: Engineering biomaterials to integrate and heal: The biocompatibility paradigm shifts. Biotechnol Bioeng. 109:1898–1911. 2012. View Article : Google Scholar : PubMed/NCBI | |
Insua A, Monje A, Wang HL and Miron RJ: Basis of bone metabolism around dental implants during osseointegration and peri-implant bone loss. J Biomed Mater Res A. 105:2075–2089. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Ferraris S, Prenesti E and Verné E: Surface functionalization of bioactive glasses with natural molecules of biological significance, part I: Gallic acid as model molecule. Appl Surf Sci. 2013. | |
Zhang X, Ferraris S, Prenesti E and Verné E: Surface functionalization of bioactive glasses with natural molecules of biological significance, part II: Grafting of polyphenols extracted from grape skin. Appl Surf Sci. 287:341–348. 2013. View Article : Google Scholar | |
Córdoba A, Satué M, Gómez-Florit M, Hierro-Oliva M, Petzold C, Lyngstadaas SP, González-Martín ML, Monjo M and Ramis JM: Flavonoid-modified surfaces: Multifunctional bioactive biomaterials with osteopromotive, anti-inflammatory, and anti-fibrotic potential. Adv Healthc Mater. 4:540–549. 2015. View Article : Google Scholar | |
Gomez-Florit M, Pacha-Olivenza MA, Fernández-Calderón MC, Córdoba A, González-Martín ML, Monjo M and Ramis JM: Quercitrin-nanocoated titanium surfaces favour gingival cells against oral bacteria. Sci Rep. 6:224442016. View Article : Google Scholar : PubMed/NCBI | |
Cazzola M, Corazzari I, Prenesti E, Bertone E, Vernè E and Ferraris S: Bioactive glass coupling with natural polyphenols: Surface modification, bioactivity and anti-oxidant ability. Appl Surf Sci. 367:237–248. 2016. View Article : Google Scholar | |
Cazzola M, Vernè E, Cochis A, Sorrentino R, Azzimonti BC, Prenesti E, Rimondini L and Ferraris S: Bioactive glasses functionalized with polyphenols: In vitro interactions with healthy and cancerous osteoblast cells. J Mater Sci. 52:2017. View Article : Google Scholar | |
Cazzola M, Ferraris S, Boschetto F, Rondinella A, Marin E, Zhu W, Pezzotti G, Vernè E and Spriano S: Green tea polyphenols coupled with a bioactive titanium alloy surface: In vitro characterization of osteoinductive behavior through a KUSA A1 cell study. Int J Mol Sci. 19:E22552018. View Article : Google Scholar : PubMed/NCBI | |
Tsuchiya S, Sugimoto K, Kamio H, Okabe K, Kuroda K, Okido M and Hibi H: Kaempferol-immobilized titanium dioxide promotes formation of new bone: Effects of loading methods on bone marrow stromal cell differentiation in vivo and in vitro. Int J Nanomedicine. 13:1665–1676. 2018. View Article : Google Scholar : PubMed/NCBI | |
Iviglia G, Bollati D, Cassinelli C, Torre E and Morra M: Dreamer: An Innovative Bone Filler Paste For The Treatment Of Periodontitis. In: Dreamer: An Innovative Bone Filler Paste For The Treatment Of Periodontitis. In: Front. Bioeng. Biotechnol. Conference Abstract: 10th World Biomaterials Congress; 2016 | |
Kallithraka S, Garcia-Viguera C, Bridle P and Bakker J: Survey of solvents for the extraction of grape seed phenolics. Phytochem Anal. 6:265–267. 1995. View Article : Google Scholar | |
Pekić B, Kovač V, Alonso E and Revilla E: Study of the extraction of proanthocyanidins from grape seeds. Food Chem. 61:201–206. 1998. View Article : Google Scholar | |
Shi J, Yu J, Pohorly J, Young JC, Bryan M and Wu Y: Optimization of the extraction of polyphenols from grape seed meal by aqueous ethanol solution. J Food Agric Environ. 1:42–47. 2003. | |
Neveu V, Perez-Jiménez J, Vos F, Crespy V, du Chaffaut L, Mennen L, Knox C, Eisner R, Cruz J, Wishart D and Scalbert A: Phenol-Explorer: An online comprehensive database on poly-phenol contents in foods. Database (Oxford). 2010. pp. bap0242010, View Article : Google Scholar | |
Rothwell JA, Urpi-Sarda M, Boto-Ordoñez M, Knox C, Llorach R, Eisner R, Cruz J, Neveu V, Wishart D, Manach C, et al: Phenol-Explorer 20: A major update of the Phenol-Explorer database integrating data on polyphenol metabolism and pharmacokinetics in humans and experimental animals. Database (Oxford). 2012. pp. bas0312012, View Article : Google Scholar | |
Rothwell JA, Pérez-Jiménez J, Neveu V, Medina-Remón A, M'hiri N, García-Lobato P, Manach C, Knox C, Eisner R, Wishart DS and Scalbert A: Phenol-Explorer 30: A major update of the Phenol-Explorer database to incorporate data on the effects of food processing on polyphenol content. Database (Oxford). 2013. pp. bat0702013, View Article : Google Scholar | |
Arumugam B, Balagangadharan K and Selvamurugan N: Syringic acid, a phenolic acid, promotes osteoblast differentiation by stimulation of Runx2 expression and targeting of Smad7 by miR-21 in mouse mesenchymal stem cells. J Cell Commun Signal. 12:561–573. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gu Q, Cai Y, Huang C, Shi Q and Yang H: Curcumin increases rat mesenchymal stem cell osteoblast differentiation but inhibits adipocyte differentiation. Pharmacogn Mag. 8:202–208. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lin SY, Kang L, Wang CZ, Huang HH, Cheng TL, Huang HT, Lee MJ, Lin YS, Ho ML, Wang GJ and Chen CH: (-)-Epigallocatechin-3-gallate (EGCG) enhances osteogenic differentiation of human bone marrow mesenchymal stem cells. Molecules. 23:E32212018. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Wu K, Xu T, Wu J, Li P, Wang H, Wu H and Wu G: Epigallocatechin-3-gallate enhances the osteoblastogenic differentiation of human adipose-derived stem cells. Drug Des Devel Ther. 13:1311–1321. 2019. View Article : Google Scholar : PubMed/NCBI | |
Song LH, Pan W, Yu YH, Quarles LD, Zhou HH and Xiao ZS: Resveratrol prevents CsA inhibition of proliferation and osteoblastic differentiation of mouse bone marrow-derived mesenchymal stem cells through an ER/NO/cGMP pathway. Toxicol In Vitro. 20:915–922. 2006. View Article : Google Scholar : PubMed/NCBI | |
Dai Z, Li Y, Quarles LD, Song T, Pan W, Zhou H and Xiao Z: Resveratrol enhances proliferation and osteoblastic differentiation in human mesenchymal stem cells via ER-dependent ERK1/2 activation. Phytomedicine. 14:806–814. 2007. View Article : Google Scholar : PubMed/NCBI | |
Wittenauer J, MäcKle S, Sußmann D, Schweiggert-Weisz U and Carle R: Inhibitory effects of polyphenols from grape pomace extract on collagenase and elastase activity. Fitoterapia. 101:179–187. 2015. View Article : Google Scholar : PubMed/NCBI | |
Brand-Williams W, Cuvelier ME and Berset C: Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol. 28:25–30. 1995. View Article : Google Scholar | |
Ribéreau-Gayon P and Stonestreet E: Determination of anthocyanins in red wine. Bull Soc Chim Fr. 9:2649–2652. 1965.In French. | |
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar | |
Hammer Ø, Harper D and Ryan P: Past: Paleontological statistics software package for education and data analysis. Paleontol Electron. 4:92001. | |
Santos J, Oliveira MB, Ibáñez E and Herrero M: Phenolic profile evolution of different ready-to-eat baby-leaf vegetables during storage. J Chromatogr A. 1327:118–131. 2014. View Article : Google Scholar : PubMed/NCBI | |
Dolan JW: Gradient Elution, Part V: Baseline Drift Problems. LCGC North Am. 31:538–543. 2013. | |
Snyder LR, Kirkland JJ and Dolan JW: Introduction to Modern Liquid Chromatography. 3rd Edition. Wiley; 2010 | |
Austermann K, Baecker N, Stehle P and Heer M: Putative effects of nutritive polyphenols on bone metabolism in vivo-evidence from human studies. Nutrients. 11:E8712019. View Article : Google Scholar : PubMed/NCBI | |
Trzeciakiewicz A, Habauzit V and Horcajada MN: When nutrition interacts with osteoblast function: Molecular mechanisms of polyphenols. Nutr Res Rev. 22:68–81. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kojima K, Maki K, Tofani I, Kamitani Y and Kimura M: Effects of grape seed proanthocyanidins extract on rat mandibular condyle. J Musculoskelet Neuronal Interact. 4:301–307. 2004.PubMed/NCBI | |
Huang JM, Bao Y, Xiang W, Jing XZ, Guo JC, Yao XD, Wang R and Guo FJ: Icariin Regulates the Bidirectional Differentiation of Bone Marrow Mesenchymal Stem Cells through Canonical Wnt Signaling Pathway. Evid Based Complement Alternat Med. 2017:80853252017. View Article : Google Scholar | |
Ma HP, Ming LG, Ge BF, Zhai YK, Song P, Xian CJ and Chen KM: Icariin is more potent than genistein in promoting osteoblast differentiation and mineralization in vitro. J Cell Biochem. 112:916–923. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hsieh TP, Sheu SY, Sun JS, Chen MH and Liu MH: Icariin isolated from Epimedium pubescens regulates osteoblasts anabolism through BMP-2, SMAD4, and Cbfa1 expression. Phytomedicine. 17:414–423. 2010. View Article : Google Scholar | |
Trzeciakiewicz A, Habauzit V, Mercier S, Barron D, Urpi-Sarda M, Manach C, Offord E and Horcajada MN: Molecular mechanism of hesperetin-7-O-glucuronide, the main circulating metabolite of hesperidin, involved in osteoblast differentiation. J Agric Food Chem. 58:668–675. 2010. View Article : Google Scholar | |
Sheng H, Zhang G, Wang X, Lee K, Yao X, Leung K, Li G and Qin L: Phytochemical molecule icariin stimulates osteogenic but inhibits adipogenic differentiation of mesenchymal stem cells. Bone. 43(Suppl 1): S42–S43. 2008. View Article : Google Scholar | |
Wei Q, Zhang J, Hong G, Chen Z, Deng W, He W and Chen MH: Icariin promotes osteogenic differentiation of rat bone marrow stromal cells by activating the ERα-Wnt/β-catenin signaling pathway. Biomed Pharmacother. 84:931–939. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tseng PC, Hou SM, Chen RJ, Peng HW, Hsieh CF, Kuo ML and Yen ML: Resveratrol promotes osteogenesis of human mesenchymal stem cells by upregulating RUNX2 gene expression via the SIRT1/FOXO3A axis. J Bone Miner Res. 26:2552–2563. 2011. View Article : Google Scholar : PubMed/NCBI | |
Dai J, Li Y, Zhou H, Chen J, Chen M and Xiao Z: Genistein promotion of osteogenic differentiation through BMP2/SMAD5/RUNX2 signaling. Int J Biol Sci. 9:1089–1098. 2013. View Article : Google Scholar : PubMed/NCBI | |
Yang L, Takai H, Utsunomiya T, Li X, Li Z, Wang Z, Wang S, Sasaki Y, Yamamoto H and Ogata Y: Kaempferol stimulates bone sialoprotein gene transcription and new bone formation. J Cell Biochem. 110:1342–1355. 2010. View Article : Google Scholar : PubMed/NCBI | |
Jung WW: Protective effect of apigenin against oxidative stress-induced damage in osteoblastic cells. Int J Mol Med. 33:1327–1334. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ying X, Sun L, Chen X, Xu H, Guo X, Chen H, Hong J, Cheng S and Peng L: Silibinin promotes osteoblast differentiation of human bone marrow stromal cells via bone morphogenetic protein signaling. Eur J Pharmacol. 721:225–230. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhao L, Wang Y, Wang Z, Xu Z, Zhang Q and Yin M: Effects of dietary resveratrol on excess-iron-induced bone loss via antioxidative character. J Nutr Biochem. 26:1174–1182. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kim JM, Lee SU, Kim YS, Min YK and Kim SH: Baicalein stimulates osteoblast differentiation via coordinating activation of MAP kinases and transcription factors. J Cell Biochem. 104:1906–1917. 2008.PubMed/NCBI | |
Liu H, Zhong L, Zhang Y, Liu X and Li J: Rutin attenuates cerebral ischemia/reperfusion injury in ovariectomized rats via estrogen receptor-mediated BDNF-TrkB and NGF-TrkA signaling. Biochem Cell Biol. 96:672–681. 2018. View Article : Google Scholar : PubMed/NCBI | |
Abdel-Naim AB, Alghamdi AA, Algandaby MM, Al-Abbasi FA, Al-Abd AM, Eid BG, Abdallah HM and El-Halawany AM: Rutin isolated from Chrozophora tinctoria enhances bone cell proliferation and ossification markers. Oxid Med Cell Longev. 2018:51064692018. View Article : Google Scholar : | |
Rassi CM, Lieberherr M, Chaumaz G, Pointillart A and Cournot G: Modulation of osteoclastogenesis in porcine bone marrow cultures by quercetin and rutin. Cell Tissue Res. 319:383–393. 2005. View Article : Google Scholar : PubMed/NCBI | |
Zhou S, Turgeman G, Harris SE, Leitman DC, Komm BS, Bodine PV and Gazit D: Estrogens activate bone morphogenetic protein-2 gene transcription in mouse mesenchymal stem cells. Mol Endocrinol. 17:56–66. 2003. View Article : Google Scholar : PubMed/NCBI | |
Hidalgo M, Sánchez-Moreno C and de Pascual-Teresa S: Flavonoid-flavonoid interaction and its effect on their antioxidant activity. Food Chem. 121:691–696. 2010. View Article : Google Scholar | |
Galanakis CM, Kotanidis A, Dianellou M and Gekas V: Phenolic content and antioxidant capacity of Cypriot wines. Czech J Food Sci. 33:126–136. 2015. View Article : Google Scholar | |
Gao J, Feng Z, Wang X, Zeng M, Liu J, Han S, Xu J, Chen L, Cao K, Long J, et al: SIRT3/SOD2 maintains osteoblast differentiation and bone formation by regulating mitochondrial stress. Cell Death Differ. 25:229–240. 2018. View Article : Google Scholar : | |
Giner M, Montoya MJ, Vázquez MA, Rios MJ, Moruno R, Miranda MJ and Pérez-Cano R: Modifying RANKL/OPG mRNA expression in differentiating and growing human primary osteoblasts. Horm Metab Res. 40:869–874. 2008. View Article : Google Scholar : PubMed/NCBI | |
Shakibaei M, Shayan P, Busch F, Aldinger C, Buhrmann C, Lueders C and Mobasheri A: Resveratrol mediated modulation of Sirt-1/Runx2 promotes osteogenic differentiation of mesenchymal stem cells: Potential role of Runx2 deacetylation. PLoS One. 7:e357122012. View Article : Google Scholar : PubMed/NCBI | |
Zhang JF, Li G, Meng CL, Dong Q, Chan CY, He ML, Leung PC, Zhang YO and Kung HF: Total flavonoids of Herba Epimedii improves osteogenesis and inhibits osteoclastogenesis of human mesenchymal stem cells. Phytomedicine. 16:521–529. 2009. View Article : Google Scholar : PubMed/NCBI | |
Marini H, Minutoli L, Polito F, Bitto A, Altavilla D, Atteritano M, Gaudio A, Mazzaferro S, Frisina A, Frisina N, et al: OPG and sRANKL serum concentrations in osteopenic, postmenopausal women after 2-year genistein administration. J Bone Miner Res. 23:715–720. 2008. View Article : Google Scholar : PubMed/NCBI | |
Napimoga MH, Clemente-Napimoga JT, Macedo CG, Freitas FF, Stipp RN, Pinho-Ribeiro FA, Casagrande R and Verri WA Jr: Quercetin inhibits inflammatory bone resorption in a mouse periodontitis model. J Nat Prod. 76:2316–2321. 2013. View Article : Google Scholar : PubMed/NCBI | |
Papadaki M, Rinotas V, Violitzi F, Thireou T, Panayotou G, Samiotaki M and Douni E: New insights for RANKL as a proinflammatory modulator in modeled inflammatory arthritis. Front Immunol. 10:972019. View Article : Google Scholar : PubMed/NCBI | |
Boyce BF, Xiu Y, Li J, Xing L and Yao Z: NF-κB-mediated regulation of osteoclastogenesis. Endocrinol Metab (Seoul). 30:35–44. 2015. View Article : Google Scholar | |
Bu SY, Lerner M, Stoecker BJ, Boldrin E, Brackett DJ, Lucas EA and Smith BJ: Dried plum polyphenols inhibit osteoclastogenesis by downregulating NFATc1 and inflammatory mediators. Calcif Tissue Int. 82:475–488. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sheu SY, Tsai CC, Sun JS, Chen MH, Liu MH and Sun MG: Stimulatory effect of puerarin on bone formation through co-activation of nitric oxide and bone morphogenetic protein-2/mitogen-activated protein kinases pathways in mice. Chin Med J (Engl). 125:3646–3653. 2012. | |
Mauney J and Volloch V: Adult human bone marrow stromal cells regulate expression of their MMPs and TIMPs in differentiation type-specific manner. Matrix Biol. 29:3–8. 2010. View Article : Google Scholar | |
Kobayashi T, Kishimoto J, Ge Y, Jin W, Hudson DL, Ouahes N, Ehama R, Shinkai H and Burgeson RE: A novel mechanism of matrix metalloproteinase-9 gene expression implies a role for keratinization. EMBO Rep. 2:604–608. 2001. View Article : Google Scholar : PubMed/NCBI | |
Philips N, Auler S, Hugo R and Gonzalez S: Beneficial regulation of matrix metalloproteinases for skin health. Enzyme Res. 2011:4272852011. View Article : Google Scholar : PubMed/NCBI | |
Garlet GP, Martins W Jr, Fonseca BA, Ferreira BR and Silva JS: Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease. J Clin Periodontol. 31:671–679. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lazăr L, Loghin A, Bud ES, Cerghizan D, Horváth E and Nagy EE: Cyclooxygenase-2 and matrix metalloproteinase-9 expressions correlate with tissue inflammation degree in periodontal disease. Rom J Morphol Embryol. 56:1441–1446. 2015. | |
Sorsa T, Mäntylä P, Tervahartiala T, Pussinen PJ, Gamonal J and Hernandez M: MMP activation in diagnostics of periodontitis and systemic inflammation. J Clin Periodontol. 38:817–819. 2011. View Article : Google Scholar : PubMed/NCBI | |
Nissinen L and Kähäri VM: Matrix metalloproteinases in inflammation. Biochim Biophys Acta. 1840:2571–2580. 2014. View Article : Google Scholar : PubMed/NCBI | |
Almalki SG and Agrawal DK: Effects of matrix metalloproteinases on the fate of mesenchymal stem cells. Stem Cell Res Ther. 7:1292016. View Article : Google Scholar : PubMed/NCBI | |
Yun JH, Pang EK, Kim CS, Yoo YJ, Cho KS, Chai JK, Kim CK and Choi SH: Inhibitory effects of green tea polyphenol (-)-epigallocatechin gallate on the expression of matrix metal-loproteinase-9 and on the formation of osteoclasts. J Periodontal Res. 39:300–307. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wang D, Wang Y, Xu S, Wang F, Wang B, Han K, Sun D and Li L: Epigallocatechin-3-gallate protects against hydrogen peroxide-induced inhibition of osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. Stem Cells Int. 2016:75327982016. View Article : Google Scholar : PubMed/NCBI | |
Gómez-Florit M, Monjo M and Ramis JM: Quercitrin for periodontal regeneration: Effects on human gingival fibroblasts and mesenchymal stem cells. Sci Rep. 5:165932015. View Article : Google Scholar : PubMed/NCBI | |
Vauzour D, Rodriguez-Mateos A, Corona G, Oruna-Concha MJ and Spencer JP: Polyphenols and human health: Prevention of disease and mechanisms of action. Nutrients. 2:1106–1131. 2010. View Article : Google Scholar : PubMed/NCBI |