Fighting for territories: Time-lapse analysis of dental pulp and dental follicle stem cells in co-culture reveals specific migratory capabilities

European Cells and Materials

Volumn 24, Issue , 2012, Pages 426-440

  Schiraldi, Chiara ^a   Stellavato, Antonietta ^a   D'Agostino, Antonella ^a   Tirino, Virginia ^a   D'Aquino, Riccardo ^a   Woloszyk, Anna ^b   De Rosa, Alfredo ^a   Laino, Luigi ^a   Papaccio, Gianpaolo ^a   Mitsiadis, Thimios A ^b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Dental follicle; Dental pulp; Dental stem cells; Odontoblast; Periodontal ligament; Regeneration; Tooth; Tooth repair

Indexed keywords

SECRETED FRIZZLED RELATED PROTEIN 1; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR RUNX2; ADAM PROTEIN; ADAM28 PROTEIN, HUMAN; MEMBRANE PROTEIN; MSX1 PROTEIN, HUMAN; NUCLEAR PROTEIN; RUNX2 PROTEIN, HUMAN; SFRP1 PROTEIN, HUMAN; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR TWIST; TWIST1 PROTEIN, HUMAN;

ADAM28 GENE; ADULT; ARTICLE; CELL ACTIVITY; CELL CULTURE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMAGE CYTOMETRY; IN VITRO STUDY; IN VIVO STUDY; MSX1 GENE; ODONTOBLAST; REAL TIME POLYMERASE CHAIN REACTION; REGULATOR GENE; RUNX2 GENE; SFRP1 GENE; STEM CELL; TIME LAPSE IMAGING; TOOTH PULP; TWIST1 GENE; UPREGULATION; CELL DIFFERENTIATION; CELL LINE; CELL MOTION; CYTOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; TOOTH SAC;

ADAM PROTEINS; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; COCULTURE TECHNIQUES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DENTAL PULP; DENTAL SAC; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MSX1 TRANSCRIPTION FACTOR; NUCLEAR PROTEINS; STEM CELLS; TRANSCRIPTION, GENETIC; TWIST TRANSCRIPTION FACTOR;

EID: 84875512732     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v024a30     Document Type: Article

References (71)

1. Aman A, Piotrowski T (2010) Cell migration during morphogenesis. Dev Biol 341: 20-33.
2. Arocena M, Zhao M, Collinson JM, Song B (2010) A time-lapse and quantitative modelling analysis of neural stem cell motion in the absence of directional cues and in electric fields. J Neurosci Res 88: 3267-3274.
3. Bai Y, Bai Y, Matsuzaka K, Hashimoto S, Kokubu E, Wang X, Inoue T (2010) Formation of bone-like tissue by dental follicle cells co-cultured with dental papilla cells. Cell Tissue Res 342: 221-231.
4. Binamé F, Pawlak G, Roux P, Hibner U (2010) What makes cells move: requirements and obstacles for spontaneous cell motility. Mol Biosyst 6: 648-661.
5. Bluteau G, Luder HU, De Bari C, Mitsiadis TA (2008) Stem cells for tooth engineering. Eur Cell Mater 16: 1-9.
6. Catón J, Bostanci N, Remboutsika E, De Bari C, Mitsiadis TA (2011) Future dentistry: cell therapy meets tooth and periodontal repair and regeneration. J Cell Mol Med 15: 1054-1065.
7. Dassule HR, McMahon AP (1998) Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol 202: 215-227.
8. d'Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G (2007) 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.
9. d'Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, Desiderio V, Laino G, Papaccio G (2009) Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cell Mater 18: 75-83.
10. d'Aquino R, Tirino V, Desiderio V, Studer M, De Angelis GC, Laino L, De Rosa A, Di Nucci D, Martino S, Paino F, Sampaolesi M, Papaccio G (2011) Human neural crest-derived postnatal cells exhibit remarkable embryonic attributes either in vitro or in vivo. Eur Cell Mater 21: 304-316.
11. Diep L, Matalova E, Mitsiadis TA, Tucker AS (2009) Contribution of the tooth bud mesenchyme to alveolar bone. J Exp Zool B Mol Dev Evol 312B: 510-517.
12. Du Y, Ling J, Wei X, Ning Y, Xie N, Gu H, Yang F (2012) Wnt/β-catenin signaling participates in cementoblast/osteoblast differentiation of dental follicle cells. Connect Tissue Res 53: 390-397.
13. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10: 445-457.
14. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, Schwartz MA (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466: 263-266.
15. Graziano A, d'Aquino R, Laino G, Proto A, Giuliano MT, Pirozzi G, De Rosa A, Di Napoli D, Papaccio G (2008) Human CD34+ stem cells produce bone nodules in vivo. Cell Prolif 41: 1-11.
16. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97: 13625-13630.
17. Handa K, Saito M, Tsunoda A, Yamauchi M, Hattori S, Sato S, Toyoda M, Teranaka T, Narayanan AS (2002) Progenitor cells from dental follicle are able to form cementum matrix in vivo. Connect Tissue Res 43: 406-408.
18. Hoffman BD, Grashoff C, Schwartz MA (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475: 316-323.
19. Huang X, Xu X, Bringas P Jr, Hung YP, Chai Y (2010) Smad4-Shh-Nfic signaling cascade-mediated epithelial-mesenchymal interaction is crucial in regulating tooth root development. J Bone Miner Res 25: 1167-1178.
20. Huth J, Buchholz M, Kraus JM, Mølhave K, Gradinaru C, v Wichert G, Gress TM, Neumann H, Kestler HA (2011) TimeLapseAnalyzer: multi-target analysis for live-cell imaging and time-lapse microscopy. Comput Methods Programs Biomed 104: 227-234.
21. Ko SO, Chung IH, Xu X, Oka S, Zhao H, Cho ES, Deng C, Chai Y (2007) Smad4 is required to regulate the fate of cranial neural crest cells. Dev Biol 312: 435-447.
22. Kuriyama S, Mayor R (2008) Molecular analysis of neural crest migration. Philos Trans R Soc Lond B Biol Sci 363: 1349-1362.
23. Laino G, d'Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G (2005) 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: 1394-1402.
24. Laird DJ, von Andrian UH, Wagers AJ (2008) Stem cell trafficking in tissue development, growth, and disease. Cell 132: 612-630.
25. Lee-MacAry AE, Ross EL, Davies D, Laylor R, Honeychurch J, Glennie MJ, Snary D, Wilkinson RW (2001) Development of a novel flow cytometric cell-mediated cytotoxicity assay using the fluorophores PKH-26 and TO-PRO-3 iodide. J Immunol Methods 252: 83-92.
26. Li J, Huang X, Xu X, Mayo J, Bringas P Jr, Jiang R, Wang S, Chai Y (2011a) SMAD4-mediated WNT signaling controls the fate of cranial neural crest cells during tooth morphogenesis. Development 138: 1977-1989.
27. Li Y, LuY, MaciejewskaI, GallerK, CavenderA, D'SouzaRN (2011b) TWIST1 promotes odontoblast differentiation. Adv Dent Res 23: 280-284.
28. Liu D, Wise GE (2007) A DNA microarray analysis of chemokine and receptor genes in the rat dental follicle--role of secreted frizzled-related protein-1 in osteoclastogenesis. Bone 41: 266-272.
29. Liu D, Yao S, Wise GE (2012) Regulation of SFRP-1 expression in the rat dental follicle. Connect Tissue Res 53: 366-372.
30. Long F (2011) Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 13: 27-38.
31. Lovschall H, Mitsiadis TA, Poulsen K, Jensen KH, Kjeldsen AL (2007) Coexpression of Notch3 and Rgs5 in the pericyte-vascular smooth muscle cell axis in response to pulp injury. Int J Dev Biol 51: 715-721.
32. Mitsiadis TA, Graf D (2009) Cell fate determination during tooth development and regeneration. Birth Defects Res C Embryo Today 87: 199-211.
33. Mitsiadis TA, Luder H (2011) Genetic basis for tooth malformations: from mice to men and back again. Clin Genet 80: 319-329.
34. Mitsiadis TA, Rahiotis C (2004) Parallels between tooth development and repair: conserved molecular mechanisms following carious and dental injury. J Dent Res 83: 896-902.
35. Mitsiadis TA, Feki A, Papaccio G, Catón J (2011) Dental pulp stem cells, niches, and notch signaling in tooth injury. Adv Dent Res 23: 275-279.
36. Mitsiadis TA, Woloszyk A, Jiménez-Rojo L (2012) Nanodentistry: combining nanostructured materials and stem cells for dental tissue regeneration. Nanomedicine 7: 1-11.
37. 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 USA 100: 5807-5812.
38. Morsczeck C, Schmalz G (2010) Transcriptomes and proteomes of dental follicle cells. J Dent Res 89: 445-456.
39. Morsczeck C, Götz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann KH (2005) Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24: 155-165.
40. Nakashima M, Iohara K (2011) Regeneration of dental pulp by stem cells. Adv Dent Res 23:313-319.
41. Okumoto S (2010) Imaging approach for monitoring cellular metabolites and ions using genetically encoded biosensors. Curr Opin Biotechnol 21: 45-54.
42. Pan K, Sun Q, Zhang J, Ge S, Li S, Zhao Y, Yang P (2010) Multilineage differentiation of dental follicle cells and the roles of RUNX2 over-expression in enhancing osteoblast/cementoblast-related gene expression in dental follicle cells. Cell Prolif 43: 219-228.
43. Papaccio G, Graziano A, d'Aquino R, Graziano MF, Pirozzi G, Menditti D, De Rosa A, Carinci F, Laino G (2006) Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated osteoblasts: a cell source for tissue repair. J Cell Physiol 208: 319-325.
44. Reichman-Fried M, Minina S, Raz E (2004) Autonomous modes of behavior in primordial germ cell migration. Dev Cell 6: 589-596.
45. Reya T, Clevers H (2005) Wnt signalling in stem cells and cancer. Nature 434: 843-850.
46. Sarkar L, Sharpe PT (2000) Inhibition of Wnt signaling by exogenous Mfrzb1 protein affects molar tooth size. J Dent Res 79: 920-925.
47. Silvério KG, Davidson KC, James RG, Adams AM, Foster BL, Nociti FH Jr, Somerman MJ, Moon RT (2012) Wnt/β-catenin pathway regulates bone morphogenetic protein (BMP2)-mediated differentiation of dental follicle cells. J Periodontal Res 47: 309-319.
48. Smith AG (2001) Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol 17: 435-462.
49. Smith GH (2005) Stem cells and mammary cancer in mice. Stem Cell Rev 1: 215-223.
50. Stephens DJ, Allan VJ (2003) Light microscopy techniques for live cell imaging. Science 300: 82-86.
51. Takeda T, Tezuka Y, Horiuchi M, Hosono K, Iida K, Hatakeyama D (2008) Characterization of dental pulp stem cells of human tooth germs. J Dent Res 87: 676-681.
52. Thesleff I, Vainio S, Jalkanen M (1989) Cell-matrix interactions in tooth development. Int J Dev Biol 33: 91-97.
53. Thesleff I, Partanen AM, Vainio S (1991) Epithelial-mesenchymal interactions in tooth morphogenesis: the roles of extracellular matrix, growth factors, and cell surface receptors. J Craniofac Genet Dev Biol 11: 229-237.
54. Thesleff I, Vaahtokari A, Partanen AM (1995) Regulation of organogenesis. Common molecular mechanisms regulating the development of teeth and other organs. Int J Dev Biol 39: 35-50.
55. Tirino V, Paino F, d'Aquino R, Desiderio V, De Rosa A, Papaccio G (2011) Methods for the identification, characterization and banking of human DPSCs: current strategies and perspectives. Stem Cell Rev 7: 608-615.
56. Vainio S, Karavanova I, Jowett A, Thesleff I (1993) Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75: 45-58.
57. Vastardis H, Karimbux N, Guthua SW, Seidman JG, Seidman CE (1996) A human MSX1 homeodomain missense mutation causes selective tooth agenesis. Nat Genet 13: 417-421.
58. Wang Y, Shyy JY, Chien S (2008) Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing. Annu Rev Biomed Eng 10: 1-38.
59. Wu J, Jin F, Tang L, Yu J, Xu L, Yang Z, Wu G, Duan Y, Jin Y (2008) Dentin non-collagenous proteins (dNCPs) can stimulate dental follicle cells to differentiate into cementoblast lineages. Biol Cell 100: 291-302.
60. Yagyuu T, Ikeda E, Ohgushi H, Tadokoro M, Hirose M, Maeda M, Inagake K, Kirita T (2010) Hard tissue-forming potential of stem/progenitor cells in human dental follicle and dental papilla. Arch Oral Biol 55: 68-76.
61. Yao S, Pan F, Prpic V, Wise GE (2008) Differentiation of stem cells in the dental follicle. J Dent Res 87: 767-771.
62. Zhao Z, Zhao M, Xiao G, Franceschi RT (2005) Gene transfer of the Runx2 transcription factor enhances osteogenic activity of bone marrow stromal cells in vitro and in vivo. Mol Ther 12: 247-253.
63. Zhao Z, Wang Y, Wang D, Liu H (2010) The regulatory role of a disintegrin and metalloproteinase 28 on the biologic property of human periodontal ligament stem cells. J Periodontol 81: 934-944.
64. Zhao Z, Watt C, Karystinou A, Roelofs AJ, McCaig CD, Gibson IR, De Bari C (2011a) Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur Cell Mater 22: 344-358.
65. Zhao Z, Liu H, Wang D (2011b) ADAM28 manipulates proliferation, differentiation, and apoptosis of human dental pulp stem cells. J Endod 37: 332-339.
66. Howard C, Murray P and Kenneth NN (2010) Dental pulp stem cell migration. J Endod 36: 1963-1966.
67. Melin M, Joffre-Romeas A, Farges JC, Couble ML, Magloire H, Bleicher F.(2000) Effects of TGFbeta1 on dental pulp cells in cultured human tooth slices. J Dent Res 79: 1689-1696.
68. Mitsiadis and Papagerakis (2011) Regenerated teeth: the future of tooth replacement? Regen Med 6: 135-139.
69. Pavasant P, Yongchaitrakul T. (2008) Secreted protein acidic, rich in cysteine induces pulp cell migration via alphavbeta3 integrin and extracellular signal-regulated kinase. Oral Dis 14: 335-430.
70. Suzuki T, Lee CH, Chen M, Zhao W, Fu SY, Qi JJ, Chotkowski G, Eisig SB, Wong A, Mao JJ. (2011) Induced migration of dental pulp stem cells for in vivo pulp regeneration. J Dent Res 90: 1013-1018.
71. Tancharoen S, Sarker KP, Imamura T, Biswas KK, Matsushita K, Tatsuyama S, Travis J, Potempa J, Torii M, Maruyama I. (2005) Neuropeptide release from dental pulp cells by RgpB via proteinase-activated receptor-2 signaling. J Immunol 174: 5796-5804.