Transplantation of Adipose-derived Cells for Periodontal Regeneration: A Systematic Review

Author(s): Dilcele Silva Moreira Dziedzic , Bassam Felipe Mogharbel , Priscila Elias Ferreira , Ana Carolina Irioda , Katherine Athayde Teixeira de Carvalho* .

Journal Name: Current Stem Cell Research & Therapy

Volume 14 , Issue 6 , 2019

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Abstract:

This systematic review evaluated the transplantation of cells derived from adipose tissue for applications in dentistry. SCOPUS, PUBMED and LILACS databases were searched for in vitro studies and pre-clinical animal model studies using the keywords “ADIPOSE”, “CELLS”, and “PERIODONTAL”, with the Boolean operator “AND”. A total of 160 titles and abstracts were identified, and 29 publications met the inclusion criteria, 14 in vitro and 15 in vivo studies. In vitro studies demonstrated that adipose- derived cells stimulate neovascularization, have osteogenic and odontogenic potential; besides adhesion, proliferation and differentiation on probable cell carriers. Preclinical studies described improvement of bone and periodontal healing with the association of adipose-derived cells and the carrier materials tested: Platelet Rich Plasma, Fibrin, Collagen and Synthetic polymer. There is evidence from the current in vitro and in vivo data indicating that adipose-derived cells may contribute to bone and periodontal regeneration. The small quantity of studies and the large variation on study designs, from animal models, cell sources and defect morphology, did not favor a meta-analysis. Additional studies need to be conducted to investigate the regeneration variability and the mechanisms of cell participation in the processes. An overview of animal models, cell sources, and scaffolds, as well as new perspectives are provided for future bone and periodontal regeneration study designs.

Keywords: Tissue engineering, cell-based therapy, adipose stem cells, bone regeneration, periodontal regeneration, systematic review.

[1]
Villar CC, Cochran DL. Regeneration of periodontal tissues: Guided tissue regeneration. Dent Clin North Am 2010; 54(1): 73-92.
[2]
Sakallioglu U, Acikgoz G, Ayas B, et al. Healing of periodontal defects treated with enamel matrix proteins and root surface conditioning--an experimental study in dogs. Biomaterials 2004; 25(10): 1831-40.
[3]
Lossdorfer S, Kraus D, Jager A. Aging affects the phenotypic characteristics of human periodontal ligament cells and the cellular response to hormonal stimulation in vitro. J Periodontal Res 2010; 45(6): 764-71.
[4]
Zhang J, An Y, Gao LN, et al. The effect of aging on the pluripotential capacity and regenerative potential of human periodontal ligament stem cells. Biomaterials 2012; 33(29): 6974-86.
[5]
Joseph J, Kapila YL, Hayami T, et al. Disease-associated extracellular matrix suppresses osteoblastic differentiation of human periodontal ligament cells via MMP-1. Calcif Tissue Int 2010; 86(2): 154-62.
[6]
Chen FM, Jin Y. Periodontal tissue engineering and regeneration: Current approaches and expanding opportunities. Tissue Eng Part B Rev 2010; 16(2): 219-55.
[7]
King GN, Hughes FJ. Bone morphogenetic protein-2 stimulates cell recruitment and cementogenesis during early wound healing. J Clin Periodontol 2001; 28(5): 465-75.
[8]
Rimondini L, Mele S. Stem cell technologies for tissue regeneration in dentistry. Minerva Stomatol 2009; 58(10): 483-500.
[9]
Akizuki T, Oda S, Komaki M, et al. Application of periodontal ligament cell sheet for periodontal regeneration: A pilot study in beagle dogs. J Periodontal Res 2005; 40(3): 245-51.
[10]
Larsson L, Decker AM, Nibali L, et al. Regenerative medicine for periodontal and peri-implant diseases. J Dent Res 2016; 95(3): 255-66.
[11]
Astolphi RD, Curbete MM, Colombo NH, et al. Periapical lesions decrease insulin signal and cause insulin resistance. J Endod 2013; 39(5): 648-52.
[12]
Colombo NH, Shirakashi DJ, Chiba FY, et al. Periodontal disease decreases insulin sensitivity and insulin signaling. J Periodontol 2012; 83(7): 864-70.
[13]
Deschner J, Eick S, Damanaki A, et al. The role of adipokines in periodontal infection and healing. Mol Oral Microbiol 2014; 29(6): 258-69.
[14]
Nokhbehsaim M, Keser S, Nogueira AV, et al. Leptin effects on the regenerative capacity of human periodontal cells. Int J Endocrinol 2014; 2014: 180304.
[15]
King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol 2008; 79(8)(Suppl.): 1527-34.
[16]
Nishimura F, Iwamoto Y, Mineshiba J, et al. Periodontal disease and diabetes mellitus: the role of tumor necrosis factor-alpha in a 2-way relationship. J Periodontol 2003; 74(1): 97-102.
[17]
Huang X, Yu T, Ma C, et al. Macrophages play a key role in the obesity-induced periodontal innate immune dysfunction via nucleotide-binding oligomerization Domain-Like Receptor Protein 3 Pathway. J Periodontol 2016; 87(10): 1195-205.
[18]
Ebersole JL, Kryscio RJ, Campbell C, et al. Salivary and serum adiponectin and C-reactive protein levels in acute myocardial infarction related to body mass index and oral health. J Periodontal Res 2017; 52(3): 419-27.
[19]
Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9(5): 641-50.
[20]
Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: In vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987; 20(3): 263-72.
[21]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[22]
Szepesi A, Matula Z, Szigeti A, et al. In vitro characterization of human mesenchymal stem cells isolated from different tissues with a potential to promote complex bone regeneration. Stem Cells Int 2016; 2016: 3595941.
[23]
De Ugarte DA, Morizono K, Elbarbary A, et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003; 174(3): 101-9.
[24]
Dragoo JL, Choi JY, Lieberman JR, et al. Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res 2003; 21(4): 622-9.
[25]
Hattori H, Sato M, Masuoka K, et al. Osteogenic potential of human adipose tissue-derived stromal cells as an alternative stem cell source. Cells Tissues Organs 2004; 178(1): 2-12.
[26]
Knippenberg M, Helder MN, Doulabi BZ, et al. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng 2005; 11(11-12): 1780-8.
[27]
Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7(2): 211-28.
[28]
Trivanovic D, Jaukovic A, Popovic B, et al. Mesenchymal stem cells of different origin: Comparative evaluation of proliferative capacity, telomere length and pluripotency marker expression. Life Sci 2015; 141: 61-73.
[29]
Hernandez-Monjaraz B, Santiago-Osorio E, Monroy-Garcia A, et al. Mesenchymal Stem Cells of dental origin for inducing tissue regeneration in periodontitis: A mini-review. Int J Mol Sci 2018; 19(4)
[30]
Sedgley CM, Botero TM. Dental stem cells and their sources. Dent Clin North Am 2012; 56(3): 549-61.
[31]
Takedachi M, Sawada K, Yamamoto S, et al. Periodontal tissue regeneration by transplantation of adipose tissue-derived stem cells. J Oral Biosci 2013; 55(3): 137-42.
[32]
Hu L, Liu Y, Wang S. Stem cell-based tooth and periodontal regeneration. Oral Dis 2018; 24(5): 696-705.
[33]
Cochran DL, Cobb CM, Bashutski JD, et al. Emerging regenerative approaches for periodontal reconstruction: A consensus report from the AAP Regeneration Workshop. J Periodontol 2015; 86(2)(Suppl.): S153-6.
[34]
Tassi SA, Sergio NZ, Misawa MYO, et al. Efficacy of stem cells on periodontal regeneration: Systematic review of pre-clinical studies. J Periodontal Res 2017; 52(5): 793-812.
[35]
Gay IC, Chen S, MacDougall M. Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res 2007; 10(3): 149-60.
[36]
Iwata T, Yamato M, Zhang Z, et al. Validation of human periodontal ligament-derived cells as a reliable source for cytotherapeutic use. J Clin Periodontol 2010; 37(12): 1088-99.
[37]
Romagnoli C, Brandi ML. Adipose mesenchymal stem cells in the field of bone tissue engineering. World J Stem Cells 2014; 6(2): 144-52.
[38]
Halvorsen YC, Wilkison WO, Gimble JM. Adipose-derived stromal cells--their utility and potential in bone formation. Int J Obes Relat Metab Disord 2000; 24(Suppl. 4): S41-4.
[39]
Halvorsen YD, Franklin D, Bond AL, et al. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 2001; 7(6): 729-41.
[40]
Kolaparthy LK, Sanivarapu S, Moogla S, et al. Adipose Tissue - adequate, accessible regenerative material. Int J Stem Cells 2015; 8(2): 121-7.
[41]
Hung CN, Mar K, Chang HC, et al. A comparison between adipose tissue and dental pulp as sources of MSCs for tooth regeneration. Biomaterials 2011; 32(29): 6995-7005.
[42]
Heo JS, Choi Y, Kim HS, et al. Comparison of molecular profiles of human mesenchymal stem cells derived from bone marrow, umbilical cord blood, placenta and adipose tissue. Int J Mol Med 2016; 37(1): 115-25.
[43]
Fraser JK, Wulur I, Alfonso Z, et al. Fat tissue: An underappreciated source of stem cells for biotechnology. Trends Biotechnol 2006; 24(4): 150-4.
[44]
Zhu Y, Liu T, Song K, et al. Adipose-derived stem cell: A better stem cell than BMSC. Cell Biochem Funct 2008; 26(6): 664-75.
[45]
Rodbell M. The metabolism of isolated fat cells. IV. Regulation of release of protein by lipolytic hormones and insulin. J Biol Chem 1966; 241(17): 3909-17.
[46]
Rodbell M. Metabolism of isolated fat cells. II. The similar effects of phospholipase C (Clostridium perfringens alpha toxin) and of insulin on glucose and amino acid metabolism. J Biol Chem 1966; 241(1): 130-9.
[47]
Rodbell M, Jones AB. Metabolism of isolated fat cells. 3. The similar inhibitory action of phospholipase C (Clostridium perfringens alpha toxin) and of insulin on lipolysis stimulated by lipolytic hormones and theophylline. J Biol Chem 1966; 241(1): 140-2.
[48]
Gagliardi C, Bunnell BA. Isolation and culture of rhesus adipose-derived stem cells. Methods Mol Biol 2011; 702: 3-16.
[49]
Locke M, Feisst V, Dunbar PR. Concise review: human adipose-derived stem cells: separating promise from clinical need. Stem Cells 2011; 29(3): 404-11.
[50]
Bunnell BA, Flaat M, Gagliardi C, et al. Adipose-derived stem cells: isolation, expansion and differentiation. Methods 2008; 45(2): 115-20.
[51]
Tholpady SS, Llull R, Ogle RC, et al. Adipose tissue: Stem cells and beyond. Clin Plast Surg 2006; 33(1): 55-62. [vi.].
[52]
Zuk P. Adipose-Derived Stem Cells in Tissue Regeneration: A Review. ISRN Stem Cells 2013; 2013: 35.
[53]
Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13(12): 4279-95.
[54]
Kishimoto N, Honda Y, Momota Y, et al. Dedifferentiated Fat (DFAT) cells: A cell source for oral and maxillofacial tissue engineering. Oral Dis 2018; 1-7.
[55]
Matsumoto T, Kano K, Kondo D, et al. Mature adipocyte-derived dedifferentiated fat cells exhibit multilineage potential. J Cell Physiol 2008; 215(1): 210-22.
[56]
Kern S, Eichler H, Stoeve J, et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006; 24(5): 1294-301.
[57]
Monaco E, Bionaz M, Hollister SJ, et al. Strategies for regeneration of the bone using porcine adult adipose-derived mesenchymal stem cells. Theriogenology 2011; 75(8): 1381-99.
[58]
Monaco E, Lima AS, Bionaz M, et al. Morphological and transcriptomic comparison of adipose and bone marrow derived porcine stem cells. J Tissue Eng Regen Med 2009; 2: 20-33.
[59]
Aust L, Devlin B, Foster SJ, et al. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 2004; 6(1): 7-14.
[60]
Yu G, Wu X, Dietrich MA, et al. Yield and characterization of subcutaneous human adipose-derived stem cells by flow cytometric and adipogenic mRNA analyzes. Cytotherapy 2010; 12(4): 538-46.
[61]
Hicok KC, Hedrick MH. Automated isolation and processing of adipose-derived stem and regenerative cells. Methods Mol Biol 2011; 702: 87-105.
[62]
Guneta V, Tan NS, Chan SK, et al. Comparative study of adipose-derived stem cells and bone marrow-derived stem cells in similar microenvironmental conditions. Exp Cell Res 2016; 348(2): 155-64.
[63]
Jurgens WJ, Oedayrajsingh-Varma MJ, Helder MN, et al. Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: Implications for cell-based therapies. Cell Tissue Res 2008; 332(3): 415-26.
[64]
Guneta V, Tan NS, Sugii S, et al. Comparative study of adipose-derived stem cells from abdomen and breast. Ann Plast Surg 2016; 76(5): 569-75.
[65]
Gronthos S, Franklin DM, Leddy HA, et al. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001; 189(1): 54-63.
[66]
Niada S, Ferreira LM, Arrigoni E, et al. Porcine adipose-derived stem cells from buccal fat pad and subcutaneous adipose tissue for future preclinical studies in oral surgery. Stem Cell Res Ther 2013; 4(6): 148.
[67]
Broccaioli E, Niada S, Rasperini G, et al. Mesenchymal Stem Cells from bichat's fat pad: In vitro comparison with adipose-derived stem cells from subcutaneous tissue. Biores Open Access 2013; 2(2): 107-7.
[68]
Bravo Cordero G, Minzer Ferrer S, Fernandez L. Odontogenic sinusitis, oro-antral fistula and surgical repair by Bichat’s fat pad: Literature review. Acta Otorrinolaringol Esp 2016; 67(2): 107-13.
[69]
Grayson WL, Bunnell BA, Martin E, et al. Stromal cells and stem cells in clinical bone regeneration. Nat Rev Endocrinol 2015; 11(3): 140-50.
[70]
Shi YY, Nacamuli RP, Salim A, et al. The osteogenic potential of adipose-derived mesenchymal cells is maintained with aging. Plast Reconstr Surg 2005; 116(6): 1686-96.
[71]
Nordberg RC, Zhang J, Griffith EH, et al. Electrical cell-substrate impedance spectroscopy can monitor age-grouped human adipose stem cell variability during osteogenic differentiation. Stem Cells Transl Med 2017; 6(2): 502-11.
[72]
Shimizu Y, Sato S. In vitro study on regeneration of periodontal tissue microvasculature using human dedifferentiated fat cells. J Periodontol 2015; 86(1): 129-36.
[73]
Akita D, Kano K, Saito-Tamura Y, et al. Use of rat mature adipocyte-derived dedifferentiated fat cells as a cell source for periodontal tissue regeneration. Front Physiol 2016; 7: 50.
[74]
Sugawara A, Sato S. Application of dedifferentiated fat cells for periodontal tissue regeneration. Hum Cell 2014; 27(1): 12-21.
[75]
Hakki SS, Turac G, Bozkurt SB, et al. Comparison of different sources of mesenchymal stem cells: Palatal versus lipoaspirated adipose tissue. Cells Tissues Organs 2017; 204(5-6): 228-40.
[76]
Kim JH, Jo CH, Kim HR, et al. Comparison of immunological characteristics of mesenchymal stem cells from the periodontal ligament, umbilical cord, and adipose tissue. Stem Cells Int 2018; 2018: 8429042.
[77]
Lee SJ, Yi T, Ahn SH, et al. Comparative study on metabolite level in tissue-specific human mesenchymal stem cells by an ultra-performance liquid chromatography quadrupole time of flight mass spectrometry. Anal Chim Acta 2018; 1024: 112-22.
[78]
Liu N, Gu B, Liu N, et al. Wnt/beta-catenin pathway regulates cementogenic differentiation of adipose tissue-deprived stem cells in dental follicle cell-conditioned medium. PLoS One 2014; 9(5): e93364.
[79]
Mattioli-Belmonte M, Teti G, Salvatore V, et al. Stem cell origin differently affects bone tissue engineering strategies. Front Physiol 2015; 6: 266.
[80]
Requicha JF, Viegas CA, Hede S, et al. Design and characterization of a biodegradable double-layer scaffold aimed at periodontal tissue-engineering applications. J Tissue Eng Regen Med 2016; 10(5): 392-403.
[81]
Requicha JF, Viegas CA, Munoz F, et al. A tissue engineering approach for periodontal regeneration based on a biodegradable double-layer scaffold and adipose-derived stem cells. Tissue Eng Part A 2014; 20(17-18): 2483-92.
[82]
Sawada K, Takedachi M, Yamamoto S, et al. Trophic factors from adipose tissue-derived multi-lineage progenitor cells promote cytodifferentiation of periodontal ligament cells. Biochem Biophys Res Commun 2015; 464(1): 299-305.
[83]
Soltani Dehnavi S, Mehdikhani M, Rafienia M, et al. Preparation and in vitro evaluation of polycaprolactone/PEG/bioactive glass nanopowders nanocomposite membranes for GTR/GBR applications. Mater Sci Eng C Mater Biol Appl 2018; 90: 236-47.
[84]
Wen X, Nie X, Zhang L, et al. Adipose tissue-deprived stem cells acquire cementoblast features treated with dental follicle cell conditioned medium containing dentin non-collagenous proteins in vitro. Biochem Biophys Res Commun 2011; 409(3): 583-9.
[85]
Xin Y, Chai G, Zhang T, et al. Analysis of multiple types of human cells subsequent to bioprinting with electrospraying technology. Biomed Rep 2016; 5(6): 723-30.
[86]
Alvira-Gonzalez J, Sanchez-Garces MA, Cairo JR, et al. Assessment of bone regeneration using adipose-derived stem cells in critical-size alveolar ridge defects: An experimental study in a dog model. Int J Oral Maxillofac Implants 2016; 31(1): 196-203.
[87]
Akita D, Morokuma M, Saito Y, et al. Periodontal tissue regeneration by transplantation of rat adipose-derived stromal cells in combination with PLGA-based solid scaffolds. Biomed Res 2014; 35(2): 91-103.
[88]
Aziz Aly LA, El-Menoufy H, Hassan A, et al. Influence of autologus adipose derived stem cells and prp on regeneration of dehiscence-type defects in alveolar bone: a comparative histochemical and histomorphometric study in dogs. Int J Stem Cells 2011; 4(1): 61-9.
[89]
Demirel S, Yalvac ME, Tapsin S, et al. Tooth replantation with adipose tissue stem cells and fibrin sealant: Microscopic analysis of rat’s teeth. Springerplus 2016; 5(1): 656.
[90]
Lemaitre M, Monsarrat P, Blasco-Baque V, et al. Periodontal tissue regeneration using syngeneic adipose-derived stromal cells in a mouse model. Stem Cells Transl Med 2017; 6(2): 656-65.
[91]
Matsubara FB, Zanicotti DG, Zielak JC, et al. Nonprocessed adipose tissue graft in the treatment of dehiscence bone defects in rabbit tibiae: a pilot study. Implant Dent 2012; 21(3): 236-41.
[92]
Sanchez-Garces MA, Alvira-Gonzalez J, Sanchez CM, et al. Bone regeneration using adipose-derived stem cells with fibronectin in dehiscence-type defects associated with dental implants: An experimental study in a dog model. Int J Oral Maxillofac Implants 2017; 32(2): e97-e106.
[93]
Shafieian R, Matin MM, Rahpeyma A, et al. The effect of platelet-rich plasma on human mesenchymal stem cell-induced bone regeneration of canine alveolar defects with calcium phosphate-based scaffolds. Iran J Basic Med Sci 2017; 20(10): 1131-40.
[94]
Tobita M, Uysal AC, Ogawa R, et al. Periodontal tissue regeneration with adipose-derived stem cells. Tissue Eng Part A 2008; 14(6): 945-53.
[95]
Tobita M, Mizuno H. Adipose-derived stem cells for periodontal tissue regeneration. Methods Mol Biol 2011; 702: 461-70.
[96]
Wu PH, Chung HY, Wang JH, et al. Amniotic membrane and adipose-derived stem cell co-culture system enhances bone regeneration in a rat periodontal defect model. J Formos Med Assoc 2016; 115(3): 186-94.
[97]
Ye L, Chen L, Feng F, et al. Bone marrow-derived stromal cells are more beneficial cell sources for tooth regeneration compared with adipose-derived stromal cells. Cell Biol Int 2015; 39(10): 1151-61.
[98]
Tobita M, Uysal CA, Guo X, et al. Periodontal tissue regeneration by combined implantation of adipose tissue-derived stem cells and platelet-rich plasma in a canine model. Cytotherapy 2013; 15(12): 1517-26.
[99]
Weinreb M, Nemcovsky CE. In vitro models for evaluation of periodontal wound healing/regeneration. Periodontol 2000 2015; 68(1): 41-54.
[100]
Lee JS, Kim TW, Park S, et al. Reduction of adipose tissue formation by the controlled release of BMP-2 using a hydroxyapatite-coated collagen carrier system for sinus-augmentation/extraction-socket grafting. Materials (Basel) 2015; 8(11): 7634-49.
[101]
Ivanovski S, Vaquette C, Gronthos S, et al. Multiphasic scaffolds for periodontal tissue engineering. J Dent Res 2014; 93(12): 1212-21.
[102]
Bartold PM, Gronthos S, Ivanovski S, et al. Tissue engineered periodontal products. J Periodontal Res 2016; 51(1): 1-15.
[103]
Donzelli E, Salvade A, Mimo P, et al. Mesenchymal stem cells cultured on a collagen scaffold: In vitro osteogenic differentiation. Arch Oral Biol 2007; 52(1): 64-73.
[104]
de Jong T, Bakker AD, Everts V, et al. The intricate anatomy of the periodontal ligament and its development: Lessons for periodontal regeneration. J Periodontal Res 2017; 52(6): 965-74.
[105]
Neo PY, Teh TK, Tay AS, et al. Stem cell-derived cell-sheets for connective tissue engineering. Connect Tissue Res 2016; 57(6): 428-42.
[106]
Hasegawa M, Yamato M, Kikuchi A, et al. Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng 2005; 11(3-4): 469-78.
[107]
Iwata T, Washio K, Yoshida T, et al. Cell sheet engineering and its application for periodontal regeneration. J Tissue Eng Regen Med 2015; 9(4): 343-56.
[108]
Kuk M, Kim Y, Lee SH, et al. Osteogenic ability of canine adipose-derived mesenchymal stromal cell sheets in relation to culture time. Cell Transplant 2016; 25(7): 1415-22.
[109]
Qian Y, Han Q, Chen W, et al. Platelet-Rich Plasma Derived Growth Factors contribute to stem cell differentiation in musculoskeletal regeneration. Front Chem 2017; 5: 89.
[110]
Pellegrini G, Seol YJ, Gruber R, et al. Pre-clinical models for oral and periodontal reconstructive therapies. J Dent Res 2009; 88(12): 1065-76.
[111]
Fawzy El-Sayed KM, Doerfer C. Animal models for periodontal tissue engineering: A knowledge generating process. Tissue Eng Part C Methods 2017; 23(12): 900-25.
[112]
Struillou X, Boutigny H, Soueidan A, et al. Experimental animal models in periodontology: a review. Open Dent J 2010; 4: 37-47.
[113]
Li H, Yan F, Lei L, et al. Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs 2009; 190(2): 94-101.
[114]
Ebina H, Hatakeyama J, Onodera M, et al. Micro-CT analysis of alveolar bone healing using a rat experimental model of critical-size defects. Oral Dis 2009; 15(4): 273-80.
[115]
Oortgiesen DA, Meijer GJ, Bronckers AL, et al. Regeneration of the periodontium using enamel matrix derivative in combination with an injectable bone cement. Clin Oral Investig 2013; 17(2): 411-21.
[116]
Oortgiesen DA, Plachokova AS, Geenen C, et al. Alkaline phosphatase immobilization onto Bio-Gide(R) and Bio-Oss(R) for periodontal and bone regeneration. J Clin Periodontol 2012; 39(6): 546-55.
[117]
Oortgiesen DA, Walboomers XF, Bronckers AL, et al. Periodontal regeneration using an injectable bone cement combined with BMP-2 or FGF-2. J Tissue Eng Regen Med 2014; 8(3): 202-9.
[118]
Levi B, James AW, Nelson ER, et al. Acute skeletal injury is necessary for human adipose-derived stromal cell-mediated calvarial regeneration. Plast Reconstr Surg 2011; 127(3): 1118-29.
[119]
Oz HS, Puleo DA. Animal models for periodontal disease. J Biomed Biotechnol 2011; 2011: 754857.
[120]
Lee JH, Lin JD, Fong JI, et al. The adaptive nature of the bone-periodontal ligament-cementum complex in a ligature-induced periodontitis rat model. Biomed Res Int 2013; 2013: 876316.
[121]
Melcher AH. Repair of wounds in the periodontium of the rat. Influence of periodontal ligament on osteogenesis. Arch Oral Biol 1970; 15(12): 1183-204.
[122]
Lekic PC, Rajshankar D, Chen H, et al. Transplantation of labeled periodontal ligament cells promotes regeneration of alveolar bone. Anat Rec 2001; 262(2): 193-202.
[123]
Talwar R, Di Silvio L, Hughes FJ, et al. Effects of carrier release kinetics on bone morphogenetic protein-2-induced periodontal regeneration in vivo. J Clin Periodontol 2001; 28(4): 340-7.
[124]
Padial-Molina M, Marchesan JT, Taut AD, et al. Methods to validate tooth-supporting regenerative therapies. Methods Mol Biol 2012; 887: 135-48.
[125]
Huang KK, Shen C, Chiang CY, et al. Effects of bone morphogenetic protein-6 on periodontal wound healing in a fenestration defect of rats. J Periodontal Res 2005; 40(1): 1-10.
[126]
Zhao M, Jin Q, Berry JE, et al. Cementoblast delivery for periodontal tissue engineering. J Periodontol 2004; 75(1): 154-61.
[127]
Iwasaki K, Komaki M, Yokoyama N, et al. Periodontal regeneration using periodontal ligament stem cell-transferred amnion. Tissue Eng Part A 2014; 20(3-4): 693-704.
[128]
Nemcovsky CE, Zahavi S, Moses O, et al. Effect of enamel matrix protein derivative on healing of surgical supra-infrabony periodontal defects in the rat molar: a histomorphometric study. J Periodontol 2006; 77(6): 996-1002.
[129]
Cai X, Yang F, Yan X, et al. Influence of bone marrow-derived mesenchymal stem cells pre-implantation differentiation approach on periodontal regeneration in vivo. J Clin Periodontol 2015; 42(4): 380-9.
[130]
Fawzy El-Sayed KM, Paris S, Becker ST, et al. Periodontal regeneration employing gingival margin-derived stem/progenitor cells: an animal study. J Clin Periodontol 2012; 39(9): 861-70.
[131]
Kim YT, Park JC, Choi SH, et al. The dynamic healing profile of human periodontal ligament stem cells: histological and immunohistochemical analysis using an ectopic transplantation model. J Periodontal Res 2012; 47(4): 514-24.
[132]
Kim K, Lee CH, Kim BK, et al. Anatomically shaped tooth and periodontal regeneration by cell homing. J Dent Res 2010; 89(8): 842-7.
[133]
d’Aquino R, De Rosa A, Lanza V, et al. Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cell Mater 2009; 18: 75-83.
[134]
Baba S, Yamada Y, Komuro A, et al. Phase I/II Trial of Autologous Bone Marrow Stem Cell Transplantation with a Three-Dimensional Woven-Fabric Scaffold for Periodontitis. Stem Cells Int 2016; 2016: 6205910.
[135]
Dufrane D, Docquier PL, Delloye C, et al. Scaffold-free three-dimensional graft from autologous adipose-derived stem cells for large bone defect reconstruction: Clinical proof of concept. Medicine (Baltimore) 2015; 94(50): e2220.
[136]
Fomekong E, Dufrane D, Berg BV, et al. Application of a three-dimensional graft of autologous osteodifferentiated adipose stem cells in patients undergoing minimally invasive transforaminal lumbar interbody fusion: clinical proof of concept. Acta Neurochir (Wien) 2017; 159(3): 527-36.
[137]
Kaku M, Akiba Y, Akiyama K, et al. Cell-based bone regeneration for alveolar ridge augmentation--cell source, endogenous cell recruitment and immunomodulatory function. J Prosthodont Res 2015; 59(2): 96-112.
[138]
Romanos GE, Asnani KP, Hingorani D, et al. PERIOSTIN: role in formation and maintenance of dental tissues. J Cell Physiol 2014; 229(1): 1-5.
[139]
Heo SC, Shin WC, Lee MJ, et al. Periostin accelerates bone healing mediated by human mesenchymal stem cell-embedded hydroxyapatite/tricalcium phosphate scaffold. PLoS One 2015; 10(3): e0116698.
[140]
Salgado AJ, Reis RL, Sousa NJ, et al. Adipose tissue derived stem cells secretome: Soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther 2010; 5: 103-10.
[141]
Shapiro IM, Landis WJ, Risbud MV. Matrix vesicles: Are they anchored exosomes? Bone 2015; 79: 29-36.
[142]
Qin Y, Sun R, Wu C, et al. Exosome: A novel approach to stimulate bone regeneration through regulation of osteogenesis and angiogenesis. Int J Mol Sci 2016; 17(5): E712.
[143]
Lu Z, Chen Y, Dunstan C, et al. Priming adipose stem cells with tumor necrosis factor-alpha preconditioning potentiates their exosome efficacy for bone regeneration. Tissue Eng Part A 2017; 23(21-22): 1212-20.
[144]
Zhang J, Liu X, Li H, et al. Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway. Stem Cell Res Ther 2016; 7(1): 136.
[145]
Wu L, Zhu F, Wu Y, et al. Dentin sialophosphoprotein-promoted mineralization and expression of odontogenic genes in adipose-derived stromal cells. Cells Tissues Organs 2008; 187(2): 103-12.
[146]
Froelich K, Steussloff G, Schmidt K, et al. DiI labeling of human adipose-derived stem cells: evaluation of DNA damage, toxicity and functional impairment. Cells Tissues Organs 2013; 197(5): 384-98.


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Article Details

VOLUME: 14
ISSUE: 6
Year: 2019
Page: [504 - 518]
Pages: 15
DOI: 10.2174/1574888X13666181105144430
Price: $58

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