Stem cells of the lamina propria of human oral mucosa and gingiva develop into mineralized tissues in vivo

Journal of Clinical Periodontology

Volumn 40, Issue 1, 2013, Pages 73-81

  Treves Manusevitz, Sandra ^a   Hoz, Lia ^b   Rachima, Heled ^c   Montoya, Gonzalo ^b   Tzur, Ephraim ^d   Vardimon, Alexander ^d   Narayanan, A Sampath ^a,e   Amar, Salomon ^f   Arzate, Higinio ^b   Pitaru, Sandu ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c SHEBA MEDICAL CENTER   (Israel)

^d ASSAF HAROFEH MEDICAL CENTER   (Israel)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f BOSTON UNIVERSITY   (United States)

Author keywords

bone; cementum; gingiva; oral mucosa; regeneration; stem cells

Indexed keywords

ALKALINE PHOSPHATASE; AMELOGENIN; BONE SIALOPROTEIN; CEMP1 PROTEIN, HUMAN; COLLAGEN; FIBRIN; OSTEOCALCIN; PROTEIN; PROTEIN TYROSINE PHOSPHATASE; PTPLA PROTEIN, HUMAN;

ANIMAL; ARTICLE; BIOSYNTHESIS; BONE REGENERATION; CEMENTUM; CYTOLOGY; GINGIVA; HUMAN; METABOLISM; MOUSE; MOUSE MUTANT; MOUTH MUCOSA; PHYSIOLOGY; REGENERATION; STEM CELL; STEM CELL TRANSPLANTATION;

ALKALINE PHOSPHATASE; AMELOGENIN; ANIMALS; BONE REGENERATION; COLLAGEN; DENTAL CEMENTUM; FIBRIN; GINGIVA; HUMANS; INTEGRIN-BINDING SIALOPROTEIN; MICE; MICE, SCID; MOUTH MUCOSA; OSTEOCALCIN; PROTEIN TYROSINE PHOSPHATASES; PROTEINS; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84870859513     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/jcpe.12016     Document Type: Article

References (37)

1. Aguilera, F. S., Osorio, E., Toledano, M., &, Osorio, R., (2011) Ultra-structure characterization of self-etching treated cementum surfaces. Medicina oral, patología oral y cirugía bucal 16, 265-270.
2. Arzate, H., Alvarez-Perez, M. A., Alvarez-Fregoso, A., Wusterhaus-Chavez, A., Reyes-Gasga, J., &, Ximenez-Fyvie, L. A., (2000) Electron microscopy, micro-analysis, and X-ray diffraction characterization of the mineral-like tissue deposited by human cementum tumor-derived cells. Journal of Dental Research 79, 28-34.
3. Bègue-Kirn, C., Krebsbach, P. H., Bartlett, J. D., &, Butler, W. T., (1998) Dentin sialoprotein, dentin phosphoprotein, enamelysin and ameloblastin: tooth-specific molecules that are distinctively expressed during murine dental differentiation. European Journal of Oral Sciences 106, 963-970.
4. Bleicher, F., Coublea, M. L., Fargesa, J. C., Coubleb, P., &, Magloirea, H., (1999) Sequential expression of matrix protein genes in developing rat teeth. Matrix Biology, 13, 3-143.
5. Bosshardt, D. D., &, Sculean, A., (2009) Does periodontal regeneration really work? Periodontology 2000 51, 208-219.
6. Bosshardt, D. D., (2008) Biological mediators and periodontal regeneration: a review of enamel matrix proteins at the cellular and molecular levels. Journal of Clinical Periodontology 35 (Suppl. 8), 87-105.
7. Davies, L. C., Locke, M., Webb, R. D., Roberts, J. T., Langley, M., Thomas, D. W., Archer, C. W., &, Stephens, P., (2010) A multipotent neural crest-derived progenitor cell population is resident within the oral mucosa lamina propria. Stem Cells and Development 19, 819-830.
8. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D. J., &, Horwitz, E., (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317.
9. Fournier, B. P., Ferre, F. C., Couty, L., Lataillade, J. J., Gourven, M., Naveau, A., Coulomb, B., Lafont, A., &, Gogly, B., (2010) Multipotent progenitor cells in gingival connective tissue. Tissue Engineering Part A 16, 2891-2899.
10. Gronthos, S., Mankani, M., Brahim, J., Robey, P. G., &, Shi, S., (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proceedings of the National Academy of Sciences of the United States of America 97, 13625-13630.
11. Haze, A., Taylor, A. L., Blumenfeld, A., Rosenfeld, E., Leiser, Y., Dafni, L., Shay, B., Gruenbaum-Cohen, Y., Fermon, E., Haegewald, S., Bernimoulin, J. P., &, Deutsch, D., (2007) Amelogenin expression in long bone and cartilage cells and in bone marrow progenitor cells. Anatomical Record 290, 455-460.
12. Hirata, A., Sugahara, T., &, Nakamura, H., (2009) Localization of runx2, osterix, and osteopontin in tooth root formation in rat molars. Journal of Histochemistry and Cytochemistry 57, 397-403.
13. Huang, G. T., Gronthos, S., &, Shi, S., (2009) Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. Journal of Dental Research 88, 792-806.
14. Karsanty, G., (2008) Transcriptional control of skeletogenesis. Annual review of genomics and human genetics 9, 183-196.
15. Lin, N. H., Gronthos, S., &, Bartold, P. M., (2009) Stem Cells and future periodontal regeneration. Periodontology 2000 51, 239-251.
16. Liu, H. W., Yakobi, R., Savion, N., Narayanan, S. A., &, Pitaru, S., (1997) A collagenous cementum attachment protein is a marker for progenitors of the mineralized tissue-forming cell lineage of the periodontal ligament. Journal of Bone and Mineral Research 12, 1691-1699.
17. Marynka-Kalmani, K., Treves, S., Yafee, M., Rachima, H., Gafni, Y., Cohen, M. A., &, Pitaru, S., (2010) The lamina propria of adult human oral mucosa harbors a novel stem cell population. Stem Cells 28, 984-995.
18. Melcher, A. H., (1976) On the repair potential of periodontal tissues. Journal of Periodontology 47, 256-260.
19. Mitrano, T. I., Grob, M. S., Carrión, F., Nova-Lamperti, E., Luz, P. A., Fierro, F. S., Quintero, A., Chaparro, A., &, Sanz, A., (2010) Culture and characterization of mesenchymal stem cells from human gingival tissue. Journal of Periodontology 81, 917-925.
20. Miura, M., Gronthos, S., Zhao, M., Lu, B., Fisher, L. W., Robey, P. G., &, Shi, S., (2003) SHED: stem cells from human exfoliated deciduous teeth. Proceedings of the National Academy of Sciences of the United States of America 100, 5807-5812.
21. Nagano, T., Oida, S., Ando, H., Gomi, K., Arai, T., &, Fukae, M., (2003) Relative levels of mRNA encoding enamel proteins in enamel organ epithelia and odontoblasts. Journal of Dental Research 82, 982-986.
22. Nuñez, J., Sanz, M., Hoz-Rodríguez, L., Zeichner-David, M., &, Arzate, H., (2010) Human cementoblasts express enamel-associated molecules in vitro and in vivo. Journal of Periodontal Research 45, 809-814.
23. Nyman, S., Gottlow, J., Karring, T., &, Lindhe, J., (1982a) The regenerative potential of the periodontal ligament. An experimental study in the monkey. Journal of Clinical Periodontology 9, 257-265.
24. Nyman, S., Lindhe, J., Karring, T., &, Rylander, H., (1982b) New attachment following surgical treatment of human periodontal disease. Journal of Clinical Periodontology 9, 290-296.
25. Rodriguez, J. P., Zavala-Alonso, V., Reyes-Vela, E., Patino-Marin, N., Ruiz, F., &, Anusavice, K. J., (2010) Atomic force microscopy observation of the enamel roughness and depth profile after phosphoric acid etching. Journal of Electron Microscopy 59, 119-125.
26. Schor, S. L., Ellis, I., Irwin, C. R., Banyard, J., Seneviratne, K., Dolman, C., Gilbert, A. D., &, Chisholm, D. M., (1996) Subpopulations of fetal-like gingival fibroblasts: Characterization and potential significance for wound healing and the progression of periodontal disease. Oral Disease 2, 155-166.
27. Seo, B. M., Miura, M., Gronthos, S., Bartold, P. M., Batouli, S., Brahim, J., Young, M., Robey, P. G., Wang, C. Y., &, Shi, S., (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364, 149-155.
28. Sonoyama, W., Liu, Y., Fang, D., Yamaza, T., Seo, B. M., Zhang, C., Liu, H., Gronthos, S., Wang, C. U., Shi, S., &, Wang, S., (2006) Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 1, e79.
29. Sonoyama, W., Liu, Y., Yamaza, T., Tuan, R. S., Wang, S., Shi, S., &, Huang, G. T. J., (2008) Characterization of apical papilla and its residing stem cells from human immature permanent teeth -A pilot study. Journal of Endontology 34, 166-171.
30. Stephens, P., Davies, K. J., Al-Khateeb, T., Shepherd, J. P., &, Thomas, D. W., (1996) A comparison of the ability of intra-oral and extra-oral fibroblasts to stimulate extracellular matrix reorganization in a model of wound contraction. Journal of Dental Research 75, 1358-1364.
31. Tang, L., Li, N., Xie, H., &, Jin, A. Y., (2011) Characterization of mesenchymal stem cells from human normal and hyperplastic gingiva. Journal of cellular physiology 226, 832-842.
32. Tomar, G. B., Srivastava, R. K., Gupta, N., Barhanpurkar, A. P., Pote, S. T., Jhaveri, H. M., Mishra, G. C., &, Wani, M. R., (2010) Human gingiva-derived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochemical and biophysical research communications 393, 377-83.
33. Venezia, E., Goldstein, M., Boyan, B. D., &, Schwartz, Z., (2004) The use of enamel matrix derivatives in the treatment of periodontal defects: a literature review and meta-analysis. Critical Review in Oral Biology and Medicine 15, 382-402.
34. Wang, F., Yu, M. J., Yan, X. L., Wen, Y., Zeng, Q., Yue, W., Yang, P., &, Pei, X,. (2011) Gingiva-derived mesenchymal stem cells-mediated therapeutic approach for bone tissue regeneration. Stem Cells and Development. 20, 2093-20102.
35. Widera, D., Zander, C., Heidbreder, M., Kasperek, Y., Noll, T., Seitz, O., Saldamli, B., Sudhoff, H., Sader, R., Kaltschmidt, C., &, Kaltschmidt, B., (2009) Adult palatum as a novel source of neural crest-related stem cells. Stem Cells 27, 1899-1910.
36. Zhang, Q., Shi, S., Liu, Y., Uyanne, J., Shi, Y., Shi, S., &, Le, A. D., (2009) Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. The Journal of Immunology 183, 7787-7798.
37. Zhou, Y., Hutmacher, D. W., Sae-Lim, V., Zhou, Z., Woodruff, M., &, Lim, T. M., (2008) Osteogenic and adipogenic induction potential of human periodontal cells. Journal of Periodontology 79, 525-534.