Comparison of periodontal ligament and gingiva-derived mesenchymal stem cells for regenerative therapies

Clinical Oral Investigations

Volumn 21, Issue 4, 2017, Pages 1095-1102

  Santamaría, Silvia ^a,b   Sanchez, Nerea ^b   Sanz, Mariano ^b   Garcia Sanz, Jose A ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Gingival; Mesenchymal stem cells; Periodontal ligament; Periodontal regeneration; Tissue engineering

Indexed keywords

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; CARCINOGENICITY; CHONDROCYTE; DIFFERENTIATION; GENETIC STABILITY; GINGIVAL BIOPSY; IN VITRO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; PERIODONTAL LIGAMENT; PHENOTYPE; REGENERATION; TISSUE ENGINEERING; TUMOR MODEL; ADOLESCENT; ADULT; ANIMAL; CELL DIFFERENTIATION; COMPARATIVE STUDY; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GINGIVA; HUMAN; MALE; MESENCHYMAL STROMA CELL; MIDDLE AGED; MOUSE; PHYSIOLOGY; PROCEDURES;

ADOLESCENT; ADULT; ANIMALS; CELL DIFFERENTIATION; FEMALE; FLOW CYTOMETRY; GINGIVA; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICE; MIDDLE AGED; PERIODONTAL LIGAMENT; PHENOTYPE; REGENERATION; TISSUE ENGINEERING;

EID: 85017697458     PISSN: 14326981     EISSN: 14363771     Source Type: Journal    
DOI: 10.1007/s00784-016-1867-3     Document Type: Article

References (46)

1. Albandar JM, Brunelle JA, Kingman A (1999) Destructive periodontal disease in adults 30 years of age and older in the United States, 1988-1994. J Periodontol 70(1):13–29. doi:10.1902/jop.1999.70.1.13
2. Lindhe J, Nyman S (1975) The effect of plaque control and surgical pocket elimination on the establishment and maintenance of periodontal health. A longitudinal study of periodontal therapy in cases of advanced disease. J Clin Periodontol 2(2):67–79
3. Esposito M, Grusovin MG, Papanikolaou N, Coulthard P, Worthington HV (2009) Enamel matrix derivative (Emdogain(R)) for periodontal tissue regeneration in intrabony defects. Cochrane Database Syst Rev 4:CD003875. doi:10.1002/14651858.CD003875.pub3
4. Needleman I, Tucker R, Giedrys-Leeper E, Worthington H (2005) Guided tissue regeneration for periodontal intrabony defects—a Cochrane Systematic Review. Periodontol 37:106–123. doi:10.1111/j.1600-0757.2004.37101.x, 2000
5. Sanz M, Tonetti MS, Zabalegui I, Sicilia A, Blanco J, Rebelo H, Rasperini G, Merli M, Cortellini P, Suvan JE (2004) Treatment of intrabony defects with enamel matrix proteins or barrier membranes: results from a multicenter practice-based clinical trial. J Periodontol 75(5):726–733. doi:10.1902/jop.2004.75.5.726
6. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147
7. Friedenstein AJ, Chailakhjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Prolif 3(4):393–403. doi:10.1111/j.1365-2184.1970.tb00347.x
8. Izadpanah R, Joswig T, Tsien F, Dufour J, Kirijan JC, Bunnell BA (2005) Characterization of multipotent mesenchymal stem cells from the bone marrow of rhesus macaques. Stem Cells Dev 14(4):440–451. doi:10.1089/scd.2005.14.440
9. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364(9429):149–155. doi:10.1016/S0140-6736(04)16627-0
10. Nunez J, Sanz-Blasco S, Vignoletti F, Munoz F, Arzate H, Villalobos C, Nunez L, Caffesse RG, Sanz M (2012) Periodontal regeneration following implantation of cementum and periodontal ligament-derived cells. J Periodontal Res 47(1):33–44. doi:10.1111/j.1600-0765.2011.01402.x
11. Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81(8):531–535
12. Tomic S, Djokic J, Vasilijic S, Vucevic D, Todorovic V, Supic G, Colic M (2011) Immunomodulatory properties of mesenchymal stem cells derived from dental pulp and dental follicle are susceptible to activation by toll-like receptor agonists. Stem Cells Dev 20(4):697–708. doi:10.1089/scd.2010.0145
13. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100(10):5807–5812. doi:10.1073/pnas.0937635100
14. Morsczeck C, Vollner F, Saugspier M, Brandl C, Reichert TE, Driemel O, Schmalz G (2010) Comparison of human dental follicle cells (DFCs) and stem cells from human exfoliated deciduous teeth (SHED) after neural differentiation in vitro. Clin Oral Investig 14(4):433–440. doi:10.1007/s00784-009-0310-4
15. Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, Huang GT (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34(2):166–171. doi:10.1016/j.joen.2007.11.021
16. Fournier BP, Ferre FC, Couty L, Lataillade JJ, Gourven M, Naveau A, Coulomb B, Lafont A, Gogly B (2010) Multipotent progenitor cells in gingival connective tissue. Tissue Eng Part A 16(9):2891–2899. doi:10.1089/ten.TEA.2009.0796
17. Mitrano TI, Grob MS, Carrion F, Nova-Lamperti E, Luz PA, Fierro FS, Quintero A, Chaparro A, Sanz A (2010) Culture and characterization of mesenchymal stem cells from human gingival tissue. J Periodontol 81(6):917–925. doi:10.1902/jop.2010.090566
18. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317. doi:10.1080/14653240600855905
19. Tomar GB, Srivastava RK, Gupta N, Barhanpurkar AP, Pote ST, Jhaveri HM, Mishra GC, Wani MR (2010) Human gingiva-derived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochem Biophys Res Commun 393(3):377–383. doi:10.1016/j.bbrc.2010.01.126
20. Kawaguchi H, Hirachi A, Hasegawa N, Iwata T, Hamaguchi H, Shiba H, Takata T, Kato Y, Kurihara H (2004) Enhancement of periodontal tissue regeneration by transplantation of bone marrow mesenchymal stem cells. J Periodontol 75(9):1281–1287. doi:10.1902/jop.2004.75.9.1281
21. Tobita M, Uysal AC, Ogawa R, Hyakusoku H, Mizuno H (2008) Periodontal tissue regeneration with adipose-derived stem cells. Tissue Eng Part A 14(6):945–953. doi:10.1089/ten.tea.2007.0048
22. Bright R, Hynes K, Gronthos S, Bartold PM (2014) Periodontal ligament-derived cells for periodontal regeneration in animal models: a systematic review. J Periodontal Res. doi:10.1111/jre.12205
23. Han J, Menicanin D, Marino V, Ge S, Mrozik K, Gronthos S, Bartold PM (2014) Assessment of the regenerative potential of allogeneic periodontal ligament stem cells in a rodent periodontal defect model. J Periodontal Res 49(3):333–345. doi:10.1111/jre.12111
24. Iwasaki K, Komaki M, Yokoyama N, Tanaka Y, Taki A, Honda I, Kimura Y, Takeda M, Akazawa K, Oda S, Izumi Y, Morita I (2014) Periodontal regeneration using periodontal ligament stem cell-transferred amnion. Tissue Eng Part A 20(3-4):693–704. doi:10.1089/ten.TEA.2013.0017
25. Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM, Gronthos S, Shi S, Wang S (2008) Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 26(4):1065–1073. doi:10.1634/stemcells.2007-0734
26. Tsumanuma Y, Iwata T, Washio K, Yoshida T, Yamada A, Takagi R, Ohno T, Lin K, Yamato M, Ishikawa I, Okano T, Izumi Y (2011) Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials 32(25):5819–5825. doi:10.1016/j.biomaterials.2011.04.071
27. Pichuantes S, Vera S, Bourdeau A, Pece N, Kumar S, Wayner EA, Letarte M (1997) Mapping epitopes to distinct regions of the extracellular domain of endoglin using bacterially expressed recombinant fragments. Tissue Antigens 50(3):265–276
28. Fujita T, Iwata T, Shiba H, Igarashi A, Hirata R, Takeda K, Mizuno N, Tsuji K, Kawaguchi H, Kato Y, Kurihara H (2007) Identification of marker genes distinguishing human periodontal ligament cells from human mesenchymal stem cells and human gingival fibroblasts. J Periodontal Res 42(3):283–286. doi:10.1111/j.1600-0765.2006.00944.x
29. Nyman S, Gottlow J, Karring T, Lindhe J (1982) The regenerative potential of the periodontal ligament. An experimental study in the monkey. J Clin Periodontol 9(3):257–265
30. Ivanovski S, Gronthos S, Shi S, Bartold PM (2006) Stem cells in the periodontal ligament. Oral Dis 12(4):358–363. doi:10.1111/j.1601-0825.2006.01253.x
31. Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Le AD (2009) Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183(12):7787–7798. doi:10.4049/jimmunol.0902318
32. Li N, Liu N, Zhou J, Tang L, Ding B, Duan Y, Jin Y (2013) Inflammatory environment induces gingival tissue-specific mesenchymal stem cells to differentiate towards a pro-fibrotic phenotype. Biol Cell 105:1–16. doi:10.1111/boc.201200064
33. Wang F, Yu M, Yan X, Wen Y, Zeng Q, Yue W, Yang P, Pei X (2011) Gingiva-derived mesenchymal stem cell-mediated therapeutic approach for bone tissue regeneration. Stem Cells Dev 20(12):2093–2102. doi:10.1089/scd.2010.0523
34. Zhang QZ, Nguyen AL, Yu WH, Le AD (2012) Human oral mucosa and gingiva: a unique reservoir for mesenchymal stem cells. J Dent Res 91(11):1011–1018. doi:10.1177/0022034512461016
35. Zhang QZ, Su WR, Shi SH, Wilder-Smith P, Xiang AP, Wong A, Nguyen AL, Kwon CW, Le AD (2010) Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells 28(10):1856–1868. doi:10.1002/stem.503
36. Jin SH, Lee JE, Yun JH, Kim I, Ko Y, Park JB (2014) Isolation and characterization of human mesenchymal stem cells from gingival connective tissue. J Periodontal Res. doi:10.1111/jre.12228
37. Mensing N, Gasse H, Hambruch N, Haeger JD, Pfarrer C, Staszyk C (2011) Isolation and characterization of multipotent mesenchymal stromal cells from the gingiva and the periodontal ligament of the horse. BMC Vet Res 7:42. doi:10.1186/1746-6148-7-42
38. Park JY, Jeon SH, Choung PH (2011) Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant 20(2):271–285. doi:10.3727/096368910X519292ct0068park
39. Gronthos S, Akintoye SO, Wang CY, Shi S (2006) Bone marrow stromal stem cells for tissue engineering. Periodontol 41:188–195. doi:10.1111/j.1600-0757.2006.00154.x, 2000
40. Tamaki Y, Nakahara T, Ishikawa H, Sato S (2013) In vitro analysis of mesenchymal stem cells derived from human teeth and bone marrow. Odontology 101(2):121–132. doi:10.1007/s10266-012-0075-0
41. Yang H, Gao LN, An Y, Hu CH, Jin F, Zhou J, Jin Y, Chen FM (2013) Comparison of mesenchymal stem cells derived from gingival tissue and periodontal ligament in different incubation conditions. Biomaterials 34(29):7033–7047. doi:10.1016/j.biomaterials.2013.05.025
42. Tang L, Li N, Xie H, Jin Y (2011) Characterization of mesenchymal stem cells from human normal and hyperplastic gingiva. J Cell Physiol 226(3):832–842. doi:10.1002/jcp.22405
43. Fawzy El-Sayed KM, Paris S, Becker ST, Neuschl M, De Buhr W, Salzer S, Wulff A, Elrefai M, Darhous MS, El-Masry M, Wiltfang J, Dorfer CE (2012) Periodontal regeneration employing gingival margin-derived stem/progenitor cells: an animal study. J Clin Periodontol 39(9):861–870. doi:10.1111/j.1600-051X.2012.01904.x
44. Li Z, Jiang CM, An S, Cheng Q, Huang YF, Wang YT, Gou YC, Xiao L, Yu WJ, Wang J (2013) Immunomodulatory properties of dental tissue-derived mesenchymal stem cells. Oral Dis. doi:10.1111/odi.12086
45. Li Z, Jiang CM, An S, Cheng Q, Huang YF, Wang YT, Gou YC, Xiao L, Yu WJ, Wang J (2014) Immunomodulatory properties of dental tissue-derived mesenchymal stem cells. Oral Dis 20(1):25–34. doi:10.1111/odi.12086
46. Zhang Q, Nguyen AL, Shi S, Hill C, Wilder-Smith P, Krasieva TB, Le AD (2012) Three-dimensional spheroid culture of human gingiva-derived mesenchymal stem cells enhances mitigation of chemotherapy-induced oral mucositis. Stem Cells Dev 21(6):937–947. doi:10.1089/scd.2011.0252