Dental pulp stem cells and bone regeneration
Amalia KAPAROU, Dimos KALYVAS, Efthymia KITRAKI
Laboratory of Basic Biomedical Sciences, School of Dentistry, National and Kapodistrian University of Athens, Greece. (Head: Professor E. Kitraki)
Hellenic Archives of Oral & Maxillofacial Surgery (2015) 1, 31-42
SUMMARY: Dental pulp, a soft tissue of mesenchymal origin, contains stem cells derived from cranial neural crest cells. Dental pulp stem cells (DPSCs) reside into special anatomic locations of dental pulp, the so called “niches”. Stem cell niches are located predominately, but not exclusively, in the perivascular regions of the pulpal cavity. DPSCs exhibit clonogenic and high proliferative activity and are capable of differentiating into several cell types. The main function of these cells is the production of tertiary/reparative dentine following trauma or caries of dental crown. Previous studies have shown that DPSCs can differentiate into osteoblast-like cells that se- crete abundant extracellular matrix and can build a woven bone in vitro. Moreover, DPSCs are capable of forming a complete and well-vascularised lamellar bone after grafting ectopically into immunocompromised rats. The in vivo transplantation of DPSCs into critical-sized bone defects in animal models has been shown to pro- mote and/or accelerate bone regeneration. These results are clearly encouraging and stress the need of further re- search for the potential clinical use of DPSCs in bone tis- sue engineering.
KEY WORDS: dental pulp, stem cells, bone defect, bone regeneration.
REFERENCES
About I, Murray PE, Franquin JC, Remusat M, Smith AJ: The effect of cavity restoration variables on odontoblast cell numbers and den- tal repair. J Dent 29(2): 109-117, 2001
Achilleos A, Trainor PA: Neural crest stem cells: discovery, properties and potential for therapy. Cell Res 22(2): 288-304, 2012
Amabile G, Meissner A: Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med 15(2): 59-68, 2009
Batouli S, Miura M, Brahim J, Tsutsui TW, Fisher LW, Gronthos S, Robey PG, Shi S: Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J Dent Res 82(12): 976-981, 2003
Bosshardt DD: Are cementoblasts a subpopulation of osteoblasts or a unique phenotype? J Dent Res 84(5): 390-406, 2005
Chai Y, Jiang X, Ito Y, Bringas P Jr, Han J, Rowitch DH, Soriano P et al: Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127(8): 1671-1679, 2000
D'Aquino R, De Rosa A, Laino G, Caruso F, Guida L, Rullo R, Checchi V et al: Human dental pulp stem cells: from biology to clinical ap- plications. J Exp Zool B Mol Dev Evol 312B(5): 408-415, 2009
D'Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, Desiderio V et al: Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cell Mater 18: 75-83, 2009
D’Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G: Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14: 1162-1171, 2007
D'Aquino R, Laino G, Papaccio G, Graziano A: Dental pulp stem cells: a promising tool for bone regeneration. Stem Cell Rev 4(1): 21- 26, 2008
Duailibi SE, Duailibi MT, Zhang W, Asrican R, Vacanti JP, Yelick PC: Bioengineered dental tissues grown in the rat jaw. J Dent Res 87(8): 745-750, 2008
García-Pacheco JM, Oliver C, Kimatrai M, Blanco FJ, Olivares EG: Human decidual stromal cells express CD34 and STRO-1 and are related to bone marrow stromal precursors. Mol Hum Re- prod 7(12): 1151-1157, 2001
Graziano A, d'Aquino R, Cusella-De Angelis MG, De Francesco F, Giordano A et al: Scaffold's surface geometry significantly affects human stem cell bone tissue engineering. J Cell Physiol 214(1): 166-172, 2008
Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A et al: Stem cell properties of human dental pulp stem cells. J Dent Res 81(8): 531-535, 2002
Gronthos S, Mankani M, Brahim J, Robey G, Shi S: Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. PNAS 97(25): 13625-13630, 2000
Goldberg M, Smith AJ: Cells and extracellular matrices of dentin and pulp: a biological basis for repair and tissue engineering. Crit Rev Oral Biol Med 15: 13–27, 2004
Huang GT, Gronthos S, Shi S: Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 88(9): 792-806, 2009
Huang GTJ, Yamaza T, Shea LD, Djouad F, Kuhn NZ, Tuan RS, Shi S: Stem/progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model. Tissue Engineering: Part A 16(2): 605-615, 2010
Ibuki N, Yamaoka Y, Sawa Y, Kawasaki T, Yoshida S: Different expres- sions of connexin 43 and 32 in the fibroblasts of human dental pulp. Tissue Cell 34(3): 170-176, 2002
Kadar K, Kiraly M, Porcsalmy B, Molnar B, Racz GZ, Blazsek J, Kallo K et al: Differentiation potential of stem cells from human dental origin- promise for tissue engineering. J Physiol Pharmacol 60(Suppl 7): 167-175, 2009
Kawashima N. Characterisation of dental pulp stem cells: a new hori- zon for tissue regeneration? Arch Oral Biol 57(11): 1439-1458, 2012
Kitagawa M, Ueda H, Iizuka S, Sakamoto K, Oka H, Kudo Y, Ogawa I et al: Immortalization and characterization of human dental pulp cells with odontoblastic differentiation. Arch Oral Biol 52(8): 727- 731, 2007
Laino G, d’Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G: A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20(8): 1394-1402, 2005
Laino G, Graziano A, d'Aquino R, Pirozzi G, Lanza V, Valiante S, De Rosa A et al: An approachable human adult stem cell source for hard-tissue engineering. J Cell Physiol 206(3): 693-701, 2006α
Laino G, Carinci F, Graziano A, d'Aquino R, Lanza V, De Rosa A, Gom- bos F et al: In vitro bone production using stem cells derived from human dental pulp. J Craniofac Surg 17(3): 511-515, 2006β
Leeb C, Jurga M, McGuckin C, Moriggl R, Kenner L: Promising new sources for pluripotent stem cells. Stem Cell Rev 6(1): 15-26, 2010
Lindroos B, Mäenpää K, Ylikomi T, Oja H, Suuronen R, Miettinen S: Characterization of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 368(2): 329-335, 2008
Liu HC, E LL, Wang DS, Su F, Wu X, Shi ZP, Lv Y, Wang JZ: Recon- struction of alveolar bone defects using bone morphogenetic pro- tein 2 mediated rabbit dental pulp stem cells seeded on nano-hy- droxyapatite/collagen/poly(L-lactide). Tissue Eng 17(19-20): 2417-
2433, Part A, 2011
Løvschall H, Tummers M, Thesleff I, Füchtbauer EM, Poulsen K: Acti- vation of the Notch signaling pathway in response to pulp capping of rat molars. Eur J Oral Sci 113(4): 312-317, 2005
Luisi SB, Barbachan JJ, Chies JA, Filho MS: Behavior of human dental pulp cells exposed to transforming growth factor-beta1 and acidic fibroblast growth factor in culture. J Endod 33(7): 833- 835, 2007
Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S: SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100(10): 5807-5812, 2003
Mitsiadis TA, Barrandon O, Rochat A, Barrandon Y, De Bari C: Stem cell niches in mammals. Exp Cell Res 313(16): 3377-3385, 2007 Morrison SJ, Shah NM, Anderson DJ: Regulatory mechanisms in stem cell biology. Cell 88(3): 287-298, 1997
Nakashima M, Iohara K, Sugiyama M: Human dental pulp stem cells with highly angiogenic and neurogenic potential for possible use in pulp regeneration. Cytokine Growth Factor Rev 20(5-6): 435- 440, 2009
Papaccio G, Graziano A, d'Aquino R, Graziano MF, Pirozzi G, Menditti D, De Rosa A, Carinci F, Laino G: Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated os- teoblasts: a cell source for tissue repair. J Cell Physiol 208(2): 319- 325, 2006
Parker GC, Anastassova-Kristeva M, Broxmeyer HE, Dodge WH, Eisenberg LM, Gehling UM: Stem cells: shibboleths of develop- ment. Stem Cells Dev 13(6): 579-584, 2004
Pierdomenico L, Bonsi L, Calvitti M, Rondelli D, Arpinati M, Chirum- bolo G, Becchetti E et al: Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80(6): 836-842, 2005
Riccio M, Maraldi T, Pisciotta A, La Sala GB, Ferrari A, Bruzzesi G, Motta A et al: Fibroin scaffold repairs critical-size bone defects in vivo supported by human amniotic fluid and dental pulp stem cells. Tissue Eng 18(9-10): 1006-1013, Part A, 2012
Rizk A, Rabie AB: Human dental pulp stem cells expressing transform- ing growth factor β3 transgene for cartilage-like tissue engineering. Cytotherapy. 2013 Mar 6. (Epub ahead of print).
Schindeler A, McDonald MM, Bokko P, Little DG: Bone remodeling during fracture repair: The cellular picture. Semin Cell Dev Biol 19(5): 459-466, 2008 Schroeder JE, Mosheiff R: Tissue engineering approaches for bone repair: Concepts and evidence. Injury 2011; in press.
Seong JM, Kim BC, Park JH, Kwon IK, Mantalaris A, Hwang YS. Stem cells in bone tissue engineering. Biomed Mater 5(6): 1-15, 2010
Shi S, Gronthos S: Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18(4): 696-704, 2003
Sloan AJ, Waddington RJ: Dental pulp stem cells: what, where, how?
Int J Paediatr Dent 19(1): 61-70, 2009
Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4): 663-676. 2006
Téclès O, Laurent P, Zygouritsas S, Burger AS, Camps J, Dejou J, About I: Activation of human dental pulp progenitor/stem cells in re- sponse to odontoblast injury. Arch Oral Biol 50(2): 103-108, 2005 Tirino V, Paino F, De Rosa A, Papaccio G: Identification, isolation, char- acterization, and banking of human dental pulp stem cells. Meth-
ods Mol Biol 879: 443-463, 2012
Tonomura A, Sumita Y, Ando Y, Iejima D, Kagami H, Honda MJ, Ueda M: Differential inducibility of human and porcine dental pulp-de- rived cells into odontoblasts. Connect Tissue Res 48(5): 229-238, 2007
Watt FM, Hogan BL: Out of Eden: stem cells and their niches. Science 287(5457): 1427-1430, 2000
Wei X, Ling J, Wu L, Liu L, Xiao Y: Expression of mineralization mark- ers in dental pulp cells. J Endod 33(6): 703-708, 2007
Yamada Y, Ito K, Nakamura S, Ueda M, Nagasaka T: Promising cell- based therapy for bone regeneration using stem cells from decid- uous teeth, dental pulp, and bone marrow. Cell Transplant 20(7): 1003-1013, 2011
Yang X, van den Dolder J, Walboomers XF, Zhang W, Bian Z, Fan M, Jansen JA: The odontogenic potential of STRO-1 sorted rat dental pulp stem cells in vitro. J Tissue Eng Regen Med 1(1): 66-73, 2007a
Yang X, Zhang W, van den Dolder J, Walboomers XF, Bian Z, Fan M, Jansen JA: Multilineage potential of STRO-1+ rat dental pulp cells in vitro. J Tissue Eng Regen Med 1(2): 128-135, 2007b
Yildirim S, Yapar M, Sermet U, Sener K, Kubar A: The role of dental pulp cells in resorption of deciduous teeth. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105(1): 113-120, 2008
Laboratory of Basic Biomedical Sciences, School of Dentistry, National and Kapodistrian University of Athens, Greece. (Head: Professor E. Kitraki)
Hellenic Archives of Oral & Maxillofacial Surgery (2015) 1, 31-42
SUMMARY: Dental pulp, a soft tissue of mesenchymal origin, contains stem cells derived from cranial neural crest cells. Dental pulp stem cells (DPSCs) reside into special anatomic locations of dental pulp, the so called “niches”. Stem cell niches are located predominately, but not exclusively, in the perivascular regions of the pulpal cavity. DPSCs exhibit clonogenic and high proliferative activity and are capable of differentiating into several cell types. The main function of these cells is the production of tertiary/reparative dentine following trauma or caries of dental crown. Previous studies have shown that DPSCs can differentiate into osteoblast-like cells that se- crete abundant extracellular matrix and can build a woven bone in vitro. Moreover, DPSCs are capable of forming a complete and well-vascularised lamellar bone after grafting ectopically into immunocompromised rats. The in vivo transplantation of DPSCs into critical-sized bone defects in animal models has been shown to pro- mote and/or accelerate bone regeneration. These results are clearly encouraging and stress the need of further re- search for the potential clinical use of DPSCs in bone tis- sue engineering.
KEY WORDS: dental pulp, stem cells, bone defect, bone regeneration.
REFERENCES
About I, Murray PE, Franquin JC, Remusat M, Smith AJ: The effect of cavity restoration variables on odontoblast cell numbers and den- tal repair. J Dent 29(2): 109-117, 2001
Achilleos A, Trainor PA: Neural crest stem cells: discovery, properties and potential for therapy. Cell Res 22(2): 288-304, 2012
Amabile G, Meissner A: Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med 15(2): 59-68, 2009
Batouli S, Miura M, Brahim J, Tsutsui TW, Fisher LW, Gronthos S, Robey PG, Shi S: Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J Dent Res 82(12): 976-981, 2003
Bosshardt DD: Are cementoblasts a subpopulation of osteoblasts or a unique phenotype? J Dent Res 84(5): 390-406, 2005
Chai Y, Jiang X, Ito Y, Bringas P Jr, Han J, Rowitch DH, Soriano P et al: Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127(8): 1671-1679, 2000
D'Aquino R, De Rosa A, Laino G, Caruso F, Guida L, Rullo R, Checchi V et al: Human dental pulp stem cells: from biology to clinical ap- plications. J Exp Zool B Mol Dev Evol 312B(5): 408-415, 2009
D'Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, Desiderio V et al: Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cell Mater 18: 75-83, 2009
D’Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G: Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14: 1162-1171, 2007
D'Aquino R, Laino G, Papaccio G, Graziano A: Dental pulp stem cells: a promising tool for bone regeneration. Stem Cell Rev 4(1): 21- 26, 2008
Duailibi SE, Duailibi MT, Zhang W, Asrican R, Vacanti JP, Yelick PC: Bioengineered dental tissues grown in the rat jaw. J Dent Res 87(8): 745-750, 2008
García-Pacheco JM, Oliver C, Kimatrai M, Blanco FJ, Olivares EG: Human decidual stromal cells express CD34 and STRO-1 and are related to bone marrow stromal precursors. Mol Hum Re- prod 7(12): 1151-1157, 2001
Graziano A, d'Aquino R, Cusella-De Angelis MG, De Francesco F, Giordano A et al: Scaffold's surface geometry significantly affects human stem cell bone tissue engineering. J Cell Physiol 214(1): 166-172, 2008
Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A et al: Stem cell properties of human dental pulp stem cells. J Dent Res 81(8): 531-535, 2002
Gronthos S, Mankani M, Brahim J, Robey G, Shi S: Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. PNAS 97(25): 13625-13630, 2000
Goldberg M, Smith AJ: Cells and extracellular matrices of dentin and pulp: a biological basis for repair and tissue engineering. Crit Rev Oral Biol Med 15: 13–27, 2004
Huang GT, Gronthos S, Shi S: Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 88(9): 792-806, 2009
Huang GTJ, Yamaza T, Shea LD, Djouad F, Kuhn NZ, Tuan RS, Shi S: Stem/progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model. Tissue Engineering: Part A 16(2): 605-615, 2010
Ibuki N, Yamaoka Y, Sawa Y, Kawasaki T, Yoshida S: Different expres- sions of connexin 43 and 32 in the fibroblasts of human dental pulp. Tissue Cell 34(3): 170-176, 2002
Kadar K, Kiraly M, Porcsalmy B, Molnar B, Racz GZ, Blazsek J, Kallo K et al: Differentiation potential of stem cells from human dental origin- promise for tissue engineering. J Physiol Pharmacol 60(Suppl 7): 167-175, 2009
Kawashima N. Characterisation of dental pulp stem cells: a new hori- zon for tissue regeneration? Arch Oral Biol 57(11): 1439-1458, 2012
Kitagawa M, Ueda H, Iizuka S, Sakamoto K, Oka H, Kudo Y, Ogawa I et al: Immortalization and characterization of human dental pulp cells with odontoblastic differentiation. Arch Oral Biol 52(8): 727- 731, 2007
Laino G, d’Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G: A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20(8): 1394-1402, 2005
Laino G, Graziano A, d'Aquino R, Pirozzi G, Lanza V, Valiante S, De Rosa A et al: An approachable human adult stem cell source for hard-tissue engineering. J Cell Physiol 206(3): 693-701, 2006α
Laino G, Carinci F, Graziano A, d'Aquino R, Lanza V, De Rosa A, Gom- bos F et al: In vitro bone production using stem cells derived from human dental pulp. J Craniofac Surg 17(3): 511-515, 2006β
Leeb C, Jurga M, McGuckin C, Moriggl R, Kenner L: Promising new sources for pluripotent stem cells. Stem Cell Rev 6(1): 15-26, 2010
Lindroos B, Mäenpää K, Ylikomi T, Oja H, Suuronen R, Miettinen S: Characterization of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 368(2): 329-335, 2008
Liu HC, E LL, Wang DS, Su F, Wu X, Shi ZP, Lv Y, Wang JZ: Recon- struction of alveolar bone defects using bone morphogenetic pro- tein 2 mediated rabbit dental pulp stem cells seeded on nano-hy- droxyapatite/collagen/poly(L-lactide). Tissue Eng 17(19-20): 2417-
2433, Part A, 2011
Løvschall H, Tummers M, Thesleff I, Füchtbauer EM, Poulsen K: Acti- vation of the Notch signaling pathway in response to pulp capping of rat molars. Eur J Oral Sci 113(4): 312-317, 2005
Luisi SB, Barbachan JJ, Chies JA, Filho MS: Behavior of human dental pulp cells exposed to transforming growth factor-beta1 and acidic fibroblast growth factor in culture. J Endod 33(7): 833- 835, 2007
Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S: SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100(10): 5807-5812, 2003
Mitsiadis TA, Barrandon O, Rochat A, Barrandon Y, De Bari C: Stem cell niches in mammals. Exp Cell Res 313(16): 3377-3385, 2007 Morrison SJ, Shah NM, Anderson DJ: Regulatory mechanisms in stem cell biology. Cell 88(3): 287-298, 1997
Nakashima M, Iohara K, Sugiyama M: Human dental pulp stem cells with highly angiogenic and neurogenic potential for possible use in pulp regeneration. Cytokine Growth Factor Rev 20(5-6): 435- 440, 2009
Papaccio G, Graziano A, d'Aquino R, Graziano MF, Pirozzi G, Menditti D, De Rosa A, Carinci F, Laino G: Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated os- teoblasts: a cell source for tissue repair. J Cell Physiol 208(2): 319- 325, 2006
Parker GC, Anastassova-Kristeva M, Broxmeyer HE, Dodge WH, Eisenberg LM, Gehling UM: Stem cells: shibboleths of develop- ment. Stem Cells Dev 13(6): 579-584, 2004
Pierdomenico L, Bonsi L, Calvitti M, Rondelli D, Arpinati M, Chirum- bolo G, Becchetti E et al: Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80(6): 836-842, 2005
Riccio M, Maraldi T, Pisciotta A, La Sala GB, Ferrari A, Bruzzesi G, Motta A et al: Fibroin scaffold repairs critical-size bone defects in vivo supported by human amniotic fluid and dental pulp stem cells. Tissue Eng 18(9-10): 1006-1013, Part A, 2012
Rizk A, Rabie AB: Human dental pulp stem cells expressing transform- ing growth factor β3 transgene for cartilage-like tissue engineering. Cytotherapy. 2013 Mar 6. (Epub ahead of print).
Schindeler A, McDonald MM, Bokko P, Little DG: Bone remodeling during fracture repair: The cellular picture. Semin Cell Dev Biol 19(5): 459-466, 2008 Schroeder JE, Mosheiff R: Tissue engineering approaches for bone repair: Concepts and evidence. Injury 2011; in press.
Seong JM, Kim BC, Park JH, Kwon IK, Mantalaris A, Hwang YS. Stem cells in bone tissue engineering. Biomed Mater 5(6): 1-15, 2010
Shi S, Gronthos S: Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18(4): 696-704, 2003
Sloan AJ, Waddington RJ: Dental pulp stem cells: what, where, how?
Int J Paediatr Dent 19(1): 61-70, 2009
Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4): 663-676. 2006
Téclès O, Laurent P, Zygouritsas S, Burger AS, Camps J, Dejou J, About I: Activation of human dental pulp progenitor/stem cells in re- sponse to odontoblast injury. Arch Oral Biol 50(2): 103-108, 2005 Tirino V, Paino F, De Rosa A, Papaccio G: Identification, isolation, char- acterization, and banking of human dental pulp stem cells. Meth-
ods Mol Biol 879: 443-463, 2012
Tonomura A, Sumita Y, Ando Y, Iejima D, Kagami H, Honda MJ, Ueda M: Differential inducibility of human and porcine dental pulp-de- rived cells into odontoblasts. Connect Tissue Res 48(5): 229-238, 2007
Watt FM, Hogan BL: Out of Eden: stem cells and their niches. Science 287(5457): 1427-1430, 2000
Wei X, Ling J, Wu L, Liu L, Xiao Y: Expression of mineralization mark- ers in dental pulp cells. J Endod 33(6): 703-708, 2007
Yamada Y, Ito K, Nakamura S, Ueda M, Nagasaka T: Promising cell- based therapy for bone regeneration using stem cells from decid- uous teeth, dental pulp, and bone marrow. Cell Transplant 20(7): 1003-1013, 2011
Yang X, van den Dolder J, Walboomers XF, Zhang W, Bian Z, Fan M, Jansen JA: The odontogenic potential of STRO-1 sorted rat dental pulp stem cells in vitro. J Tissue Eng Regen Med 1(1): 66-73, 2007a
Yang X, Zhang W, van den Dolder J, Walboomers XF, Bian Z, Fan M, Jansen JA: Multilineage potential of STRO-1+ rat dental pulp cells in vitro. J Tissue Eng Regen Med 1(2): 128-135, 2007b
Yildirim S, Yapar M, Sermet U, Sener K, Kubar A: The role of dental pulp cells in resorption of deciduous teeth. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105(1): 113-120, 2008
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