Formation and Developmental Specification of the Odontogenic and Osteogenic Mesenchymes

. 2020 ; 8 () : 640. [epub] 20200717

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid32850793

Within the mandible, the odontogenic and osteogenic mesenchymes develop in a close proximity and form at about the same time. They both originate from the cranial neural crest. These two condensing ecto-mesenchymes are soon separated from each other by a very loose interstitial mesenchyme, whose cells do not express markers suggesting a neural crest origin. The two condensations give rise to mineralized tissues while the loose interstitial mesenchyme, remains as a soft tissue. This is crucial for proper anchorage of mammalian teeth. The situation in all three regions of the mesenchyme was compared with regard to cell heterogeneity. As the development progresses, the early phenotypic differences and the complexity in cell heterogeneity increases. The differences reported here and their evolution during development progressively specifies each of the three compartments. The aim of this review was to discuss the mechanisms underlying condensation in both the odontogenic and osteogenic compartments as well as the progressive differentiation of all three mesenchymes during development. Very early, they show physical and structural differences including cell density, shape and organization as well as the secretion of three distinct matrices, two of which will mineralize. Based on these data, this review highlights the consecutive differences in cell-cell and cell-matrix interactions, which support the cohesion as well as mechanosensing and mechanotransduction. These are involved in the conversion of mechanical energy into biochemical signals, cytoskeletal rearrangements cell differentiation, or collective cell behavior.

Zobrazit více v PubMed

Alemi A. S., Mazur C. M., Fowler T. M., Woo J. J., Knott P. D., Alliston T. (2018). Glucocorticoids cause mandibular bone fragility and suppress osteocyte perilacunar-canalicular remodeling. Bone Rep. 9 145–153. 10.1016/j.bonr.2018.09.004 PubMed DOI PMC

Alfaqeeh S. A., Gaete M., Tucker A. S. (2013). Interactions of the tooth and bone during development. J. Dent. Res. 92 1129–1135. 10.1177/0022034513510321 PubMed DOI

Allard B., Magloire H., Couble M. L., Maurin J. C., Bleicher F. (2006). Voltage-gated sodium channels confer excitability to human odontoblasts: possible role in tooth pain transmission. J. Biol. Chem. 281 29002–29010. 10.1074/jbc.M601020200 PubMed DOI

Amorim B. R., Silvério K. G., Casati M. Z., Sallum E. A., Kantovitz K. R., Nociti F. H., Jr. (2016). Neuropilin controls endothelial differentiation by mesenchymal stem cells from the periodontal ligament. J. Periodontol. 87 e138–e147. 10.1902/jop.2016.150603 PubMed DOI

Andrade C. M., Roesch G. C., Wink M. R., Guimarães E. L., Souza L. F., Jardim F. R., et al. (2008). Activity and expression of ecto-5’-nucleotidase/CD73 are increased during phenotype conversion of a hepatic stellate cell line. Life Sci. 82 21–29. 10.1016/j.lfs.2007.10.003 PubMed DOI

Bae Y. K., Kim G. H., Lee J. C., Seo B. M., Joo K. M., Lee G., et al. (2017). The significance of SDF-1α-CXCR4 axis in in vivo angiogenic ability of human periodontal ligament stem cells. Mol. Cells 40 386–392. 10.14348/molcells.2017.0004 PubMed DOI PMC

Beertsen W., McCulloch C. A., Sodek J. (1997). The periodontal ligament: a unique, multifunctional connective tissue. Periodontology 13 20–40. 10.1111/j.1600-0757.1997.tb00094.x PubMed DOI

Berendsen A. D., Olsen B. R. (2015). Bone development. Bone 80 14–18. 10.1016/j.bone.2015.04.035 PubMed DOI PMC

Bidder M., Latifi T., Towler D. A. (1998). Reciprocal temporospatial patterns of Msx2 and Osteocalcin gene expression during murine odontogenesis. J. Bone. Miner. Res. 13 609–619. 10.1359/jbmr.1998.13.4.609 PubMed DOI

Bishop M. A. (1987). An investigation of pulp capillaries and tight junctions between odontoblasts in cats. Anat. Embryol. 177 131–138. 10.1007/BF00572537 PubMed DOI

Bobek J., Oralova V., Lesot H., Kratochvilova A., Doubek J., Matalova E. (2020). Onset of calciotropic receptors during the initiation of mandibular/alveolar bone formation. Ann. Anat. 227:151427. 10.1016/j.aanat.2019.151427 PubMed DOI

Bonewald L. F., Johnson M. L. (2008). Osteocytes, mechanosensing and Wnt signaling. Bone 42 606–615. 10.1016/j.bone.2007.12.224 PubMed DOI PMC

Boskey A. L. (1998). Biomineralization: conflicts, challenges, and opportunities. J. Cell Biochem. Suppl. 30-31 83–91. 10.1002/(sici)1097-4644(1998)72:30/31+<83::aid-jcb12>3.0.co;2-f PubMed DOI

Boyce B. F., Xing L. (2007). Biology of RANK, RANKL, and osteoprotegerin. Arthritis Res. Ther. 9(Suppl. 1), S1. 10.1186/ar2165 PubMed DOI PMC

Burger E. H., Klein-Nulend J. (1999). Mechanotransduction in bone–role of the lacuno-canalicular network. FASEB J. 13(Suppl.) S101–S112. PubMed

Burghardt A. J., Link T. M., Majumdar S. (2011). High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin. Orthop Relat. Res. 469 2179–2193. 10.1007/s11999-010-1766-x PubMed DOI PMC

Byers M. R. (1984). Dental sensory receptors. Int. Rev. Neurobiol. 25 39–94. 10.1016/s0074-7742(08)60677-7 PubMed DOI

Byers M. R., Maeda T., Brown A. M., Westenbroek R. E. (2004). GFAP immunoreactivity and transcription in trigeminal and dental tissues of rats and transgenic GFP/GFAP mice. Microsc. Res. Tech. 65 295–307. 10.1002/jemt.20130 PubMed DOI

Byun J. H., Lee J. H., Choi Y. J., Kim J. R., Park B. W. (2008). Co-expression of nerve growth factor and p75NGFR in the inferior alveolar nerve after mandibular distraction osteogenesis. Int. J. Oral Maxillofac. Surg. 37 467–472. 10.1016/j.ijom.2008.01.017 PubMed DOI

Campagnola P. J., Millard A. C., Terasaki M., Hoppe P. E., Malone C. J., Mohler W. A. (2002). Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. Biophys. J. 82 493–508. 10.1016/S0006-3495(02)75414-3 PubMed DOI PMC

Casagrande L., Demarco F. F., Zhang Z., Araujo F. B., Shi S., Nör J. E. (2010). Dentin-derived BMP-2 and odontoblast differentiation. J. Dent. Res. 89 603–608. 10.1177/0022034510364487 PubMed DOI

Chai Y., Jiang X., Ito Y., Bringas P., Jr., Han J., Rowitch D. H., et al. (2000). Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127 1671–1679. PubMed

Cho M. I., Garant P. R. (2000). Development and general structure of the periodontium. Periodontol. 2000 24 9–27. 10.1034/j.1600-0757.2000.2240102.x PubMed DOI

Clark K., Langeslag M., van Leeuwen B., Ran L., Ryazanov A. G., Figdor C. G., et al. (2006). TRPM7, a novel regulator of actomyosin contractility and cell adhesion. EMBO J. 25 290–301. 10.1038/sj.emboj.7600931 PubMed DOI PMC

Corpron R. E., Avery J. K. (1973). The ultrastructure of intradental nerves in developing mouse molars. Anat. Rec. 175 585–606. 10.1002/ar.1091750307 PubMed DOI

Costello M. J., Brennan L. A., Mohamed A., Gilliland K. O., Johnsen S., Kantorow M. (2016). Identification and ultrastructural characterization of a novel nuclear degradation complex in differentiating lens fiber cells. PLoS One 11:e0160785. 10.1371/journal.pone.0160785 PubMed DOI PMC

Dallas S. L., Bonewald L. F. (2010). Dynamics of the transition from osteoblast to osteocyte. Ann. N. Y. Acad. Sci. 1192 437–443. 10.1111/j.1749-6632.2009.05246.x PubMed DOI PMC

Dangaria S. J., Ito Y., Luan X., Diekwisch T. G. (2011). Differentiation of neural-crest-derived intermediate pluripotent progenitors into committed periodontal populations involves unique molecular signature changes, cohort shifts, and epigenetic modifications. Stem Cells Dev. 20 39–52. 10.1089/scd.2010.0180 PubMed DOI PMC

Dangaria S. J., Ito Y., Walker C., Druzinsky R., Luan X., Diekwisch T. G. H. (2009). Extracellular matrix-mediated differentiation of periodontal progenitor cells. Differentiation 78 79–90. 10.1016/j.diff.2009.03.005 PubMed DOI PMC

Dassule H. R., McMahon A. P. (1998). Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev. Biol. 202 215–227. 10.1006/dbio.1998.8992 PubMed DOI

Denk W., Horstmann H. (2004). Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2:e329. 10.1371/journal.pbio.0020329 PubMed DOI PMC

Diekwisch T. G. (2002). Pathways and fate of migratory cells during late tooth organogenesis. Connect. Tissue Res. 43 245–256. PubMed

Diep L., Matalova E., Mitsiadis T. A., Tucker A. S. (2009). Contribution of the tooth bud mesenchyme to alveolar bone. J. Exp. Zool. B Mol. Dev. Evol. 312B 510–517. 10.1002/jez.b.21269 PubMed DOI

Discher D. E., Janmey P., Wang Y. L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310 1139–1143. 10.1126/science.1116995 PubMed DOI

Dunlop L. L., Hall B. K. (1995). Relationships between cellular condensation, preosteoblast formation and epithelial-mesenchymal interactions in initiation of osteogenesis. Int. J. Dev. Biol. 39 357–371. PubMed

Epelman S., Lavine K. J., Randolph G. J. (2014). Origin and functions of tissue macrophages. Immunity 41 21–35. 10.1016/j.immuni.2014.06.013 PubMed DOI PMC

Everts V., Delaisse J. M., Korper W., Jansen D. C., Tigchelaar-Gutter W., Saftig P., et al. (2002). The bone lining cell: its role in cleaning Howship’s lacunae and initiating bone formation. J. Bone Miner. Res. 17 77–90. 10.1359/jbmr.2002.17.1.77 PubMed DOI

Farahani R. M., Sarrafpour B., Simonian M., Li Q., Hunter N. (2012). Directed glia-assisted angiogenesis in a mature neurosensory structure: pericytes mediate an adaptive response in human dental pulp that maintains blood-barrier function. J. Comp. Neurol. 520 3803–3826. 10.1002/cne.23162 PubMed DOI

Farges J. C., Romeas A., Melin M., Pin J. J., Lebecque S., Lucchini M., et al. (2003). TGF-beta1 induces accumulation of dendritic cells in the odontoblast layer. J. Dent. Res. 82 652–656. 10.1177/154405910308200816 PubMed DOI

Farhadieh R. D., Nicklin S., Yu Y., Gianoutsos M. P., Walsh W. R. (2003). The role of nerve growth factor and brain-derived neurotrophic factor in inferior alveolar nerve regeneration in distraction osteogenesis. J. Craniofac. Surg. 14 859–865. 10.1097/00001665-200311000-00007 PubMed DOI

Feng J., Mantesso A., De Bari C., Nishiyama A., Sharpe P. T. (2011). Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc. Natl. Acad. Sci. U.S.A. 108 6503–6508. 10.1073/pnas.1015449108 PubMed DOI PMC

Ferguson J. W., Atit R. P. (2019). A tale of two cities: the genetic mechanisms governing calvarial bone development. Genesis 57:e23248. 10.1002/dvg.23248 PubMed DOI PMC

Fleischmannova J., Matalova E., Sharpe P. T., Misek I., Radlanski R. J. (2010). Formation of the tooth-bone interface. J. Dent. Res. 89 108–115. 10.1177/0022034509355440 PubMed DOI

Foster B. L., Ao M., Salmon C. R., Chavez M. B., Kolli T. N., Tran A. B., et al. (2018). Osteopontin regulates dentin and alveolar bone development and mineralization. Bone 107 196–207. 10.1016/j.bone.2017.12.004 PubMed DOI PMC

Franz-Odendaal T. A. (2011). Induction and patterning of intramembranous bone. Front. Biosci. 16 2734–2746. 10.2741/3882 PubMed DOI

Fujiyama K., Yamashiro T., Fukunaga T., Balam T. A., Zheng L., Takano-Yamamoto T. (2004). Denervation resulting in dento-alveolar ankylosis associated with decreased Malassez epithelium. J. Dent. Res. 83 625–629. 10.1177/154405910408300808 PubMed DOI

Gauthier P., Yu Z., Tran Q. T., Bhatti F. U., Zhu X., Huang G. T. (2017). Cementogenic genes in human periodontal ligament stem cells are downregulated in response to osteogenic stimulation while upregulated by vitamin C treatment. Cell Tissue Res. 368 79–92. 10.1007/s00441-016-2513-8 PubMed DOI PMC

Giffin J. L., Gaitor D., Franz-Odendaal T. A. (2019). The forgotten skeletogenic condensations: a comparison of early skeletal development amongst vertebrates. J. Dev. Biol. 7:4. 10.3390/jdb7010004 PubMed DOI PMC

Goldberg M., Farges J. C., Lacerda-Pinheiro S., Six N., Jegat N., Decup F., et al. (2008). Inflammatory and immunological aspects of dental pulp repair. Pharmacol. Res. 58 137–147. 10.1016/j.phrs.2008.05.013 PubMed DOI PMC

Grandfield K., Herber R. P., Chen L., Djomehri S., Tam C., Lee J. H., et al. (2015). Strain-guided mineralization in the bone-PDL-cementum complex of a rat periodontium. Bone Rep. 3 20–31. 10.1016/j.bonr.2015.04.002 PubMed DOI PMC

Griffin F. E., Schiavi J., McDevitt T. C., McGarry J. P., McNamara L. M. (2017). The role of adhesion junctions in the biomechanical behaviour and osteogenic differentiation of 3D mesenchymal stem cell spheroids. J. Biomech. 59 71–79. 10.1016/j.jbiomech.2017.05.014 PubMed DOI PMC

Groetsch A., Gourrier A., Schwiedrzik J., Sztucki M., Beck R. J., Shephard J. D., et al. (2019). Compressive behaviour of uniaxially aligned individual mineralised collagen fibres at the micro- and nanoscale. Acta Biomater. 89 313–329. 10.1016/j.actbio.2019.02.053 PubMed DOI

Grosso A., Burger M. G., Lunger A., Schaefer D. J., Banfi A., Di Maggio N. (2017). It takes two to tango: coupling of angiogenesis and osteogenesis for bone regeneration. Front. Bioeng. Biotechnol. 5:68. 10.3389/fbioe.2017.00068 PubMed DOI PMC

Guntur A. R., Rosen C. J., Naski M. C. (2012). N-cadherin adherens junctions mediate osteogenesis through PI3K signaling. Bone 50 54–62. 10.1016/j.bone.2011.09.036 PubMed DOI PMC

Hakki S. S., Wang D., Franceschi R. T., Somerman M. J. (2006). Bone sialoprotein gene transfer to periodontal ligament cells may not be sufficient to promote mineralization in vitro or in vivo. J. Periodontol. 77 167–173. 10.1902/jop.2006.050057 PubMed DOI

Hall B. K. (1980). Tissue interactions and the initiation of osteogenesis and chondrogenesis in the neural crest-derived mandibular skeleton of the embryonic mouse as seen in isolated murine tissues and in recombinations of murine and avian tissues. J. Embryol. Exp. Morphol. 58 251–264. PubMed

Hall B. K., Miyake T. (1995). Divide, accumulate, differentiate: cell condensation skeletal development. Int. J. Dev. Biol. 39 881–893. PubMed

Hall B. K., Miyake T. (2000). All for one and one for all: condensations and the initiation of skeletal development. Bioessays 22 138–147. 10.1002/(sici)1521-1878(200002)22:2<138::aid-bies5>3.0.co;2-4 PubMed DOI

Hayashi M., Nakashima T., Taniguchi M., Kodama T., Kumanogoh A., Takayanagi H. (2012). Osteoprotection by semaphorin 3A. Nature 485 69–74. 10.1038/nature11000 PubMed DOI

He J., Zhang N., Zhang J., Jiang B., Wu F. (2018). Migration critically meditates osteoblastic differentiation of bone mesenchymal stem cells through activating canonical Wnt signal pathway. Coll. Surf. B Biointerfaces 171 205–213. 10.1016/j.colsurfb.2018.07.017 PubMed DOI

Hill C., Jacobs B., Kennedy L., Rohde S., Zhou B., Baldwin S., et al. (2015). Cranial neural crest deletion of VEGFa causes cleft palate with aberrant vascular and bone development. Cell Tissue Res. 361 711–722. 10.1007/s00441-015-2150-7 PubMed DOI

Hill E. L., Elde R. (1991). Distribution of CGRP-, VIP-, D beta H-, SP-, and NPY-immunoreactive nerves in the periosteum of the rat. Cell Tissue Res. 264 469–480. 10.1007/BF00319037 PubMed DOI

Hirashima S., Kanazawa T., Ohta K., Nakamura K. I. (2020a). Three-dimensional ultrastructural analysis and histomorphometry of collagen bundles in the periodontal ligament using focused ion beam/scanning electron microscope tomography. J. Periodont. Res. 55 23–23. 10.1111/jre.12592 PubMed DOI

Hirashima S., Kanazawa T., Ohta K., Nakamura K. I. (2020b). Three-dimensional ultrastructural imaging and quantitative analysis of the periodontal ligament. Anat. Sci. Int. 95 1–11. 10.1007/s12565-019-00502-5 PubMed DOI

Ho S. P., Marshall S. J., Ryder M. I., Marshall G. W. (2007). The tooth attachment mechanism defined by structure, chemical composition and mechanical properties of collagen fibers in the periodontium. Biomaterials 28 5238–5245. 10.1016/j.biomaterials.2007.08.031 PubMed DOI PMC

Hu B., Nadiri A., Bopp-Kuchler S., Perrin-Schmitt F., Wang S., Lesot H. (2005). Dental epithelial histo-morphogenesis in the mouse: positional information versus cell history. Arch. Oral. Biol. 50 131–136. 10.1016/j.archoralbio.2004.09.007 PubMed DOI

Huang W., Yang S., Shao J., Li Y. P. (2007). Signaling and transcriptional regulation in osteoblast commitment and differentiation. Front. Biosci. 12 3068–3092. 10.2741/2296 PubMed DOI PMC

Huang Y. H., Ohsaki Y., Kurisu K. (1991). Distribution of type I and type III collagen in the developing periodontal ligament of mice. Matrix 11 25–35. 10.1016/s0934-8832(11)80224-6 PubMed DOI

Jabalee J., Hillier S., Franz-Odendaal T. A. (2013). An investigation of cellular dynamics during the development of intramembranous bones: the scleral ossicles. J. Anat. 223 311–320. 10.1111/joa.12095 PubMed DOI PMC

Javed A., Chen H., Ghori F. Y. (2010). Genetic and transcriptional control of bone formation. Oral Maxillofac. Surg. Clin. North Am. 22 283–293. 10.1016/j.coms.2010.05.001 PubMed DOI PMC

Jones R. E., Salhotra A., Robertson K. S., Ransom R. C., Foster D. S., Shah H. N., et al. (2019). Skeletal stem cell-schwann cell circuitry in mandibular repair. Cell Rep. 28 2757–2766. 10.1016/j.celrep.2019.08.021 PubMed DOI PMC

Jontell M., Okiji T., Dahlgren U., Bergenholtz G. (1998). Immune defense mechanisms of the dental pulp. Crit. Rev. Oral Biol. Med. 9 179–200. 10.1177/10454411980090020301 PubMed DOI

Kaneko T., Okiji T., Kaneko R., Suda H. (2008). Characteristics of resident dendritic cells in various regions of rat periodontal ligament. Cell Tissue Res. 331 413–421. 10.1007/s00441-007-0539-7 PubMed DOI

Keller L., Kökten T., Kuchler-Bopp S., Lesot H. (2015). “Tooth organ engineering,” in Stem Cell Biology and Tissue Engineering in Dental Sciences, eds Vishwakarma A., Sharpe P., Shi S., Wang X.-P., Ramalingam M. (Cambridge, MA: Academic Press; ) 359–368. 10.1016/B978-0-12-397157-9.00032-1 DOI

Keller L. V., Kuchler-Bopp S., Lesot H. (2012). Restoring physiological cell heterogeneity in the mesenchyme during tooth engineering. Int. J. Dev. Biol. 56 737–746. 10.1387/ijdb.120076hl PubMed DOI

Keller L. V., Kuchler-Bopp S., Mendoza S. A., Poliard A., Lesot H. (2011). Tooth engineering: searching for dental mesenchymal cells sources. Front. Physiol. 2:7. 10.3389/fphys.2011.00007 PubMed DOI PMC

Kenan S., Onur ÖD., Solakoðlu S., Kotil T., Ramazanoðlu M., Çelik H. H., et al. (2019). Investigation of the effects of semaphorin 3A on new bone formation in a rat calvarial defect model. J. Craniomaxillofac. Surg. 47 473–483. 10.1016/j.jcms.2018.12.010 PubMed DOI

Kerschnitzki M., Wagermaier W., Roschger P., Seto J., Shahar R., Duda G. N., et al. (2011). The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J. Struct. Biol. 173 303–311. 10.1016/j.jsb.2010.11.014 PubMed DOI

Kjaer I. (1990). Correlated appearance of ossification and nerve tissue in human fetal jaws. J. Craniofac. Genet. Dev. Biol. 10 329–336. PubMed

Kokten T., Bécavin T., Keller L., Weickert J. L., Kuchler-Bopp S., Lesot H. (2014a). Immunomodulation stimulates the innervation of engineered tooth organ. PLoS One 9:e86011. 10.1371/journal.pone.0086011 PubMed DOI PMC

Kokten T., Lesot H., Kuchler-Bopp S. (2014b). “Experimental design for the innervation of tooth forming from implanted cell re-associations,” in Cells and Biomaterials in Regenerative Medicine, ed. Eberli D. (Rijeka: InTech Open Access Publisher; ), 345–373.

Komatsu N., Kajiya M., Motoike S., Takewaki M., Horikoshi S., Iwata T., et al. (2018). Type I collagen deposition via osteoinduction ameliorates YAP/TAZ activity in 3D floating culture clumps of mesenchymal stem cell/extracellular matrix complexes. Stem Cell Res. Ther. 9:342. 10.1186/s13287-018-1085-9 PubMed DOI PMC

Krivanek J., Adameyko I., Fried K. (2017). Heterogeneity and developmental connections between cell types inhabiting teeth. Front. Physiol. 8:376. 10.3389/fphys.2017.00376 PubMed DOI PMC

Kuchler-Bopp S., Keller L., Poliard A., Lesot H. (2011). “Tooth organ engineering: biological constraints specifying experimental approaches,” in Tissue Engineering for Tissue and Organ Regeneration, ed. Eberli D. (London: InTech; ), 317–346. 10.5772/23483 DOI

Ladoux B., Mège R. M. (2017). Mechanobiology of collective cell behaviours. Nat. Rev. Mol. Cell Biol. 18 743–757. 10.1038/nrm.2017.98 PubMed DOI

Lausch A. J., Quan B. D., Miklas J. W., Sone E. D. (2013). Extracellular matrix control of collagen mineralization in vitro. Adv. Funct. Mater. 23 4906–4912. 10.1002/adfm.201203760 DOI

Lecanda F., Warlow P. M., Sheikh S., Furlan F., Steinberg T. H., Civitelli R. (2000). Connexin43 deficiency causes delayed ossification, craniofacial abnormalities, and osteoblast dysfunction. J. Cell Biol. 151 931–944. 10.1083/jcb.151.4.931 PubMed DOI PMC

Ledesma-Martínez E., Mendoza-Núñez V. M., Santiago-Osorio E. (2016). Mesenchymal stem cells derived from dental pulp: a review. Stem Cells Int. 2016:4709572. 10.1155/2016/4709572 PubMed DOI PMC

Lee J. H., Pryce B. A., Schweitzer R., Ryder M., I, Ho S. P. (2015). Differentiating zones at periodontal ligament-bone and periodontal ligament-cementum entheses. J. Periodontal Res. 50 870–880. 10.1111/jre.12281 PubMed DOI PMC

Lekic P., McCulloch C. A. (1996). Relationship of cellular proliferation to expression of osteopontin and bone sialoprotein in regenerating rat periodontium. Cell Tissue Res. 285 491–500. 10.1007/s004410050665 PubMed DOI

Leong N. L., Hurng J. M., Djomehri S. I., Gansky S. A., Ryder M. I., Ho S. P. (2012). Age-related adaptation of bone-PDL-tooth complex: rattus-norvegicus as a model system. PLoS One 7:e35980. 10.1371/journal.pone.0035980 PubMed DOI PMC

Lin H., Liu H., Sun Q., Yuan G., Zhang L., Chen Z. (2013). KLF4 promoted odontoblastic differentiation of mouse dental papilla cells via regulation of DMP1. J. Cell. Physiol. 228 2076–2085. 10.1002/jcp.24377 PubMed DOI

Lin H., Xu L., Liu H., Sun Q., Chen Z., Yuan G., et al. (2011). KLF4 promotes the odontoblastic differentiation of human dental pulp cells. J Endod. 37 948–954. 10.1016/j.joen.2011.03.030 PubMed DOI

Linde A. (1995). Dentin mineralization and the role of odontoblasts in calcium transport. Connect. Tissue Res. 33 163–170. 10.3109/03008209509016997 PubMed DOI

Liu Y. S., Liu Y. A., Huang C. J., Yen M. H., Tseng C. T., Chien S., et al. (2015). Mechanosensitive TRPM7 mediates shear stress and modulates osteogenic differentiation of mesenchymal stromal cells through Osterix pathway. Sci. Rep. 5:16522. 10.1038/srep16522 PubMed DOI PMC

Luan X., Ito Y., Dangaria S., Diekwisch T. G. (2006). Dental follicle progenitor cell heterogeneity in the developing mouse periodontium. Stem Cells Dev. 15 595–608. 10.1089/scd.2006.15.595 PubMed DOI PMC

Lumsden A. G. (1988). Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103(Suppl.) 155–169. PubMed

Lungova V., Radlanski R. J., Tucker A. S., Renz H., Misek I., Matalova E. (2011). Tooth-bone morphogenesis during postnatal stages of mouse first molar development. J. Anat. 218 699–716. 10.1111/j.1469-7580.2011.01367.x PubMed DOI PMC

Luukko K., Kettunen P. (2014). Coordination of tooth morphogenesis and neuronal development through tissue interactions: lessons from mouse models. Exp. Cell Res. 325 72–77. 10.1016/j.yexcr.2014.02.029 PubMed DOI

Luukko K., Kettunen P. (2016). Integration of tooth morphogenesis and innervation by local tissue interactions, signaling networks, and semaphorin 3A. Cell Adh. Migr. 10 618–626. 10.1080/19336918.2016.1216746 PubMed DOI PMC

MacDonald M. E., Hall B. K. (2001). Altered timing of the extracellular-matrix-mediated epithelial-mesenchymal interaction that initiates mandibular skeletogenesis in three inbred strains of mice: development, heterochrony, and evolutionary change in morphology. J. Exp. Zool. 291 258–273. 10.1002/jez.1102.abs PubMed DOI

MacNeil R. L., Thomas H. F. (1993). Development of the murine periodontium. II. Role of the epithelial root sheath in formation of the periodontal attachment. J. Periodontol. 64 285–291. 10.1902/jop.1993.64.4.285 PubMed DOI

Maeda Y., Miwa Y., Sato I. (2017). Expression of CGRP, vasculogenesis and osteogenesis associated mRNAs in the developing mouse mandible and tibia. Ann. Anat. 221 38–47. 10.4081/ejh.2017.2750 PubMed DOI PMC

Magloire H., Couble M. L., Thivichon-Prince B., Maurin J. C., Bleicher F. (2009). Odontoblast: a mechano-sensory cell. J. Exp. Zool. B Mol. Dev. Evol. 312B 416–424. 10.1002/jez.b.21264 PubMed DOI

Magloire H., Maurin J. C., Couble M. L., Shibukawa Y., Tsumura M., Thivichon-Prince B., et al. (2010). Topical review. Dental pain and odontoblasts: facts and hypotheses. J. Orofac. Pain 24 335–349. PubMed

Mammoto T., Mammoto A., Ingber D. E. (2013). Mechanobiology and developmental control. Annu. Rev. Cell Dev. Biol. 29 27–61. 10.1146/annurev-cellbio-101512-122340 PubMed DOI

Mammoto T., Mammoto A., Jiang A., Jiang E., Hashmi B., Ingber D. E. (2015). Mesenchymal condensation-dependent accumulation of collagen VI stabilizes organ-specific cell fates during embryonic tooth formation. Dev. Dyn. 244 713–723. 10.1002/dvdy.24264 PubMed DOI PMC

Mammoto T., Mammoto A., Torisawa Y. S., Tat T., Gibbs A., Derda R., et al. (2011). Mechanochemical control of mesenchymal condensation and embryonic tooth organ formation. Dev. Cell 21 758–769. 10.1016/j.devcel.2011.07.006 PubMed DOI PMC

Martin T. J. (2005). Osteoblast-derived PTHrP is a physiological regulator of bone formation. J. Clin. Invest. 115 2322–2324. 10.1172/JCI26239 PubMed DOI PMC

Matheson S., Larjava H., Häkkinen L. (2005). Distinctive localization and function for lumican, fibromodulin and decorin to regulate collagen fibril organization in periodontal tissues. J. Periodontal Res. 40 312–324. 10.1111/j.1600-0765.2005.00800.x PubMed DOI

McKee M. D., Hoac B., Addison W. N., Barros N. M., Millán J. L., Chaussain C. (2013). Extracellular matrix mineralization in periodontal tissues: noncollagenous matrix proteins, enzymes, and relationship to hypophosphatasia and X-linked hypophosphatemia. Periodontol. 2000 63 102–122. 10.1111/prd.12029 PubMed DOI PMC

McKee M. D., Nanci A. (1996). Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc. Res. Tech. 3 141–164. 10.1002/(sici)1097-0029(19960201)33:2<141::aid-jemt5>3.0.co;2-w PubMed DOI

McKeown S. J., Newgreen D. F., Farlie P. G. (2005). Dlx2 over-expression regulates cell adhesion and mesenchymal condensation in ectomesenchyme. Dev. Biol. 281 22–37. 10.1016/j.ydbio.2005.02.004 PubMed DOI

Miletich I., Sharpe P. T. (2003). Normal and abnormal dental development. Hum. Mol. Genet. 12 R69–R73. 10.1093/hmg/ddg085 PubMed DOI

Mina M., Kollar E. J. (1987). The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch. Oral. Biol. 32 123–127. 10.1016/0003-9969(87)90055-0 PubMed DOI

Minkoff R., Rundus V. R., Parker S. B., Hertzberg E. L., Laing J. G., Beyer E. C. (1994). Gap junction proteins exhibit early and specific expression during intramembranous bone formation in the developing chick mandible. Anat. Embryol. 190 231–241. 10.1007/BF00234301 PubMed DOI

Moe K., Kettunen P., Kvinnsland I. H., Luukko K. (2008). Development of the pioneer sympathetic innervation into the dental pulp of the mouse mandibular first molar. Arch. Oral. Biol. 53 865–873. 10.1016/j.archoralbio.2008.03.004 PubMed DOI

Moe K., Sijaona A., Shrestha A., Kettunen P., Taniguchi M., Luukko K. (2012). Semaphorin 3A controls timing and patterning of the dental pulp innervation. Differentiation 84 371–379. 10.1016/j.diff.2012.09.003 PubMed DOI

Moorer M. C., Hebert C., Tomlinson R. E., Iyer S. R., Chason M., Stains J. P. (2017). Defective signaling, osteoblastogenesis and bone remodeling in a mouse model of connexin 43 C-terminal truncation. J. Cell Sci. 130 531–540. 10.1242/jcs.197285 PubMed DOI PMC

Nait Lechguer A., Kuchler-Bopp S., Hu B., Haïkel Y., Lesot H. (2008). Vascularization of engineered teeth. J. Dent. Res. 87 1138–1143. 10.1177/154405910808701216 PubMed DOI

Nakagawa N., Kinosaki M., Yamaguchi K., Shima N., Yasuda H., Yano K., et al. (1998). RANK is the essential signaling receptor for osteoclast differentiation factor in osteoclastogenesis. Biochem. Biophys. Res. Commun. 253 395–400. 10.1006/bbrc.1998.9788 PubMed DOI

Nakamura H., Nakashima T., Hayashi M., Izawa N., Yasui T., Aburatani H., et al. (2014). Global epigenomic analysis indicates protocadherin-7 activates osteoclastogenesis by promoting cell-cell fusion. Biochem. Biophys. Res. Commun. 455 305–311. 10.1016/j.bbrc.2014.11.009 PubMed DOI

Nakatomi M., Hovorakova M., Gritli-Linde A., Blair H. J., MacArthur K., Peterka M., et al. (2013). Evc regulates a symmetrical response to Shh signaling in molar development. J. Dent. Res. 92 222–228. 10.1177/0022034512471826 PubMed DOI

Nanci A., Wazen R., Nishio C., Zalzal S. F. (2008). Immunocytochemistry of matrix proteins in calcified tissues: functional biochemistry on section. Eur. J. Histochem. 52 201–214. 10.4081/1218 PubMed DOI

Nava M. M., Raimondi M. T., Pietrabissa R. (2012). Controlling self-renewal and differentiation of stem cells via mechanical cues. J. Biomed. Biotechnol. 2012:797410. 10.1155/2012/797410 PubMed DOI PMC

Ng T. K., Yang Q., Fortino V. R., Lai N. Y., Carballosa C. M., Greenberg J. M., et al. (2019). MicroRNA-132 directs human periodontal ligament-derived neural crest stem cell neural differentiation. J. Tissue Eng. Regen. Med. 13 12–24. 10.1002/term.2759 PubMed DOI

Obara N., Lesot H. (2007). Asymmetrical growth, differential cell proliferation, and dynamic cell rearrangement underlie epithelial morphogenesis in mouse molar development. Cell Tissue Res. 330 461–473. 10.1007/s00441-007-0502-7 PubMed DOI

Okiji T., Jontell M., Belichenko P., Bergenholtz G., Dahlström A. (1997). Perivascular dendritic cells of the human dental pulp. Acta Physiol. Scand. 159 163–169. 10.1046/j.1365-201X.1997.584337000.x PubMed DOI

Okiji T., Kawashima N., Kosaka T., Matsumoto A., Kobayashi C., Suda H. (1992). An immunohistochemical study of the distribution of immunocompetent cells, especially macrophages and Ia antigen-expressing cells of heterogeneous populations, in normal rat molar pulp. J. Dent. Res 71 1196–1202. 10.1177/00220345920710051201 PubMed DOI

Orsini G., Ruggeri A., Jr., Mazzoni A., Papa V., Mazzotti G., Di Lenarda R., et al. (2007). Immunohistochemical identification of decorin and biglycan in human dentin: a correlative field emission scanning electron microscopy/transmission electron microscopy study. Calcif. Tissue Int. 81 39–45. 10.1007/s00223-007-9027-z PubMed DOI

Osborn J. W., Price D. G. (1988). An autoradiographic study of periodontal development in the mouse. J. Dent. Res. 67 455–461. 10.1177/00220345880670020401 PubMed DOI

Oster G. F., Murray J. D., Harris A. K. (1983). Mechanical aspects of mesenchymal morphogenesis. J. Embryol. Exp. Morphol. 78 83–125. PubMed

Paris M., Götz A., Hettrich I., Bidan C. M., Dunlop J. W. C., Razi H., et al. (2017). Scaffold curvature-mediated novel biomineralization process originates a continuous soft tissue-to-bone interface. Acta Biomater. 60 64–80. 10.1016/j.actbio.2017.07.029 PubMed DOI

Radlanski R. J., Renz H., Zimmermann C. A., Mey R., Matalova E. (2015). Morphogenesis of the compartmentalizing bone around the molar primordia in the mouse mandible during dental developmental stages between lamina, bell-stage, and root formation (E13-P20). Ann. Anat. 200 1–14. 10.1016/j.aanat.2015.01.003 PubMed DOI

Ray P., Chapman S. C. (2015). Cytoskeletal reorganization drives mesenchymal condensation and regulates downstream molecular signaling. PLoS One 10:e0134702. 10.1371/journal.pone.0134702 PubMed DOI PMC

Reichenberger E., Baur S., Sukotjo C., Olsen B. R., Karimbux N. Y., Nishimura I. (2000). Collagen XII mutation disrupts matrix structure of periodontal ligament and skin. J. Dent. Res. 79 1962–1968. 10.1177/00220345000790120701 PubMed DOI

Ricard-Blum S. (2011). The collagen family. Cold Spring Harb. Perspect. Biol. 3:a004978. 10.1101/cshperspect.a004978 PubMed DOI PMC

Roguljic H., Matthews B. G., Yang W., Cvija H., Mina M., Kalajzic I. (2013). In vivo identification of periodontal progenitor cells. J. Dent. Res. 92 709–715. 10.1177/0022034513493434 PubMed DOI PMC

Rothova M., Feng J., Sharpe P. T., Peterkova R., Tucker A. S. (2011). Contribution of mesoderm to the developing dental papilla. Int. J. Dev. Biol. 55 59–64. 10.1387/ijdb.103083mr PubMed DOI

Rothova M., Peterkova R., Tucker A. S. (2012). Fate map of the dental mesenchyme: dynamic development of the dental papilla and follicle. Dev. Biol. 366 244–254. 10.1016/j.ydbio.2012.03.018 PubMed DOI

Ruch J. V. (1998). Odontoblast commitment and differentiation. Biochem. Cell Biol. 76 923–938. 10.1139/o99-008 PubMed DOI

Ruch J. V., Lesot H., Bègue-Kirn C. (1995). Odontoblast differentiation. Int. J. Dev. Biol. 39 51–68. PubMed

Ruch J. V., Lesot H., Karcher-Djuricic V., Meyer J. M., Olive M. (1982). Facts and hypotheses concerning the control of odontoblast differentiation. Differentiation 21 7–12. 10.1111/j.1432-0436.1982.tb01187.x PubMed DOI

Saghiri M. A., Asatourian A., Sorenson C. M., Sheibani N. (2018). Mice dental pulp and periodontal ligament endothelial cells exhibit different proangiogenic properties. Tissue Cell. 50 31–36. 10.1016/j.tice.2017.11.004 PubMed DOI PMC

Santagati F., Rijli F. M. (2003). Cranial neural crest and the building of the vertebrate head. Nat. Rev. Neurosci. 4 806–818. 10.1038/nrn1221 PubMed DOI

Sawakami K., Robling A. G., Ai M., Pitner N. D., Liu D., Warden S. J., et al. (2006). The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J. Biol. Chem. 281 23698–23711. 10.1074/jbc.M601000200 PubMed DOI

Seo B. M., Miura M., Gronthos S., Bartold P. M., Batouli S., Brahim J., et al. (2004). Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364 149–155. 10.1016/S0140-6736(04)16627-0 PubMed DOI

Shahar R., Weiner S. (2018). Open questions on the 3D structures of collagen containing vertebrate mineralized tissues: a perspective. J. Struct. Biol. 201 187–198. 10.1016/j.jsb.2017.11.008 PubMed DOI

Sharpe P. T. (2016). Dental mesenchymal stem cells. Development 143 2273–2280. 10.1242/dev.134189 PubMed DOI

Shi S., Bartold P. M., Miura M., Seo B. M., Robey P. G., Gronthos S. (2005). The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod. Craniofac. Res. 8 191–199. 10.1111/j.1601-6343.2005.00331.x PubMed DOI

Shinagawa-Ohama R., Mochizuki M., Tamaki Y., Suda N., Nakahara T. (2017). Heterogeneous human periodontal ligament-committed progenitor and stem cell populations exhibit a unique cementogenic property under in vitro and in vivo conditions. Stem Cells Dev. 26 632–645. 10.1089/scd.2016.0330 PubMed DOI

Shyer A. E., Rodrigues A. R., Schroeder G. G., Kassianidou E., Kumar S., Harland R. M. (2017). Emergent cellular self-organization and mechanosensation initiate follicle pattern in the avian skin. Science 357 811–815. 10.1126/science.aai7868 PubMed DOI PMC

Silver F. H., Horvath I., Foran D. J. (2002). Mechanical implications of the domain structure of fiber-forming collagens: comparison of the molecular and fibrillar flexibilities of the alpha1-chains found in types I-III collagen. J. Theor. Biol. 216 243–254. 10.1006/jtbi.2002.2542 PubMed DOI

Steitz S. A., Speer M. Y., McKee M. D., Liaw L., Almeida M., Yang H., et al. (2002). Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am. J. Pathol. 161 2035–2046. 10.1016/S0002-9440(10)64482-3 PubMed DOI PMC

Sun Y., Chen C. S., Fu J. (2012). Forcing stem cells to behave: a biophysical perspective of the cellular microenvironment. Annu. Rev. Biophys. 41 519–542. 10.1146/annurev-biophys-042910-155306 PubMed DOI PMC

Suphasiriroj W., Mikami M., Sato S. (2013). Comparative studies on microvascular endothelial cells isolated from periodontal tissue. J. Periodontol. 84 1002–1009. 10.1902/jop.2012.120453 PubMed DOI

Tabata S., Ozaki H. S., Nakashima M., Uemura M., Iwamoto H. (1998). Innervation of blood vessels in the rat incisor pulp: a scanning electron microscopic and immunoelectron microscopic study. Anat. Rec. 251 384–391. 10.1002/(sici)1097-0185(199807)251:3<384::aid-ar14>3.0.co;2-k PubMed DOI

Takebe T., Enomura M., Yoshizawa E., Kimura M., Koike H., Ueno Y., et al. (2015). Vascularized and complex organ buds from diverse tissues via mesenchymal cell-driven condensation. Cell Stem Cell. 16 556–565. 10.1016/j.stem.2015.03.004 PubMed DOI

Ten Cate A. R. (1997). The development of the periodontium–a largely ectomesenchymally derived unit. Periodontol. 2000 13 9–19. 10.1111/j.1600-0757.1997.tb00093.x PubMed DOI

Thesleff I., Vaahtokari A., Kettunen P., Aberg T. (1995). Epithelial-mesenchymal signaling during tooth development. Connect. Tissue Res. 32 9–15. 10.3109/03008209509013700 PubMed DOI

Thesleff I., Vaahtokari A., Vainio S., Jowett A. (1996). Molecular mechanisms of cell and tissue interactions during early tooth development. Anat. Rec. 245 151–161. 10.1002/(sici)1097-0185(199606)245:2<151::aid-ar4>3.0.co;2-# PubMed DOI

Tomokiyo A., Wada N., Maeda H. (2019). Periodontal ligament stem cells: regenerative potency in periodontium. Stem Cells Dev. 28 974–985. 10.1089/scd.2019.0031 PubMed DOI

Tomokiyo A., Yoshida S., Hamano S., Hasegawa D., Sugii H., Maeda H. (2018). Detection, characterization, and clinical application of mesenchymal stem cells in periodontal ligament tissue. Stem Cells Int. 2018:5450768. 10.1155/2018/5450768 PubMed DOI PMC

Trubiani O., Pizzicannella J., Caputi S., Marchisio M., Mazzon E., Paganelli R., et al. (2019). Periodontal ligament stem cells: current knowledge and future perspectives. Stem Cells Dev. 28 995–1003. 10.1089/scd.2019.0025 PubMed DOI

Vainio S., Thesleff I. (1992). Sequential induction of syndecan, tenascin and cell proliferation associated with mesenchymal cell condensation during early tooth development. Differentiation 50 97–105. 10.1111/j.1432-0436.1992.tb00490.x PubMed DOI

Vesela B., Svandova E., Bobek J., Lesot H., Matalova E. (2019). Osteogenic and angiogenic profiles of mandibular bone-forming cells. Front. Physiol. 10:124. 10.3389/fphys.2019.00124 PubMed DOI PMC

Volponi A. A., Sharpe P. T. (2013). The tooth – a treasure chest of stem cells. Br. Dent. J. 215 353–358. 10.1038/sj.bdj.2013.959 PubMed DOI

Wada N., Maeda H., Hasegawa D., Gronthos S., Bartold P. M., Menicanin D., et al. (2014). Semaphorin 3A induces mesenchymal-stem-like properties in human periodontal, ligament cells. Stem Cells Dev. 23 2225–2236. 10.1089/scd.2013.0405 PubMed DOI PMC

Wada N., Menicanin D., Shi S., Bartold P. M., Gronthos S. (2009). Immunomodulatory properties of human periodontal ligament stem cells. J. Cell. Physiol. 219 667–676. 10.1002/jcp.21710 PubMed DOI

Wang L., Foster B. L., Kram V., Nociti F. H., Jr., Zerfas P. M., Tran A. B., et al. (2014). Fibromodulin and biglycan modulate periodontium through TGFβ/BMP signaling. J. Dent. Res. 93 780–787. 10.1177/0022034514541126 PubMed DOI PMC

Wang Y., Wan C., Deng L., Liu X., Cao X., Gilbert S. R., et al. (2007). The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J. Clin. Invest. 117 1616–1626. 10.1172/JCI31581 PubMed DOI PMC

Wu X., Shi W., Cao X. (2007). Multiplicity of BMP signaling in skeletal development. Ann. N. Y. Acad. Sci. 1116 29–49. 10.1196/annals.1402.053 PubMed DOI

Xu R. (2014). Semaphorin 3A: a new player in bone remodeling. Cell Adh. Migr. 8 5–10. 10.4161/cam.27752 PubMed DOI PMC

Yamada S., Tomoeda M., Ozawa Y., Yoneda S., Terashima Y., Ikezawa K., et al. (2007). PLAP-1/asporin, a novel negative regulator of periodontal ligament mineralization. J. Biol. Chem. 282 23070–23080. 10.1074/jbc.M611181200 PubMed DOI

Yamamoto N., Maeda H., Tomokiyo A., Fujii S., Wada N., Monnouchi S., et al. (2012). Expression and effects of glial cell line-derived neurotrophic factor on periodontal ligament cells. J. Clin. Periodontol. 39 556–564. 10.1111/j.1600-051X.2012.01881.x PubMed DOI

Yamaza T., Ren G., Akiyama K., Chen C., Shi Y., Shi S. (2011). Mouse mandible contains distinctive mesenchymal stem cells. J. Dent. Res. 90 317–324. 10.1177/0022034510387796 PubMed DOI PMC

Yang N., Li Y., Wang G., Ding Y., Jin Y., Xu Y. (2017). Tumor necrosis factor-α suppresses adipogenic and osteogenic differentiation of human periodontal ligament stem cell by inhibiting miR-21/Spry1 functional axis. Differentiation 97 33–43. 10.1016/j.diff.2017.08.004 PubMed DOI

Yavropoulou M. P., Yovos J. G. (2016). The molecular basis of bone mechanotransduction. J. Musculoskelet. Neuronal. Interact. 16 221–236. PubMed PMC

Yeasmin S., Ceccarelli J., Vigen M., Carrion B., Putnam A. J., Tarle S. A., et al. (2014). Stem cells derived from tooth periodontal ligament enhance functional angiogenesis by endothelial cells. Tissue Eng. Part A 20 1188–1196. 10.1089/ten.TEA.2013.0512 PubMed DOI PMC

Yegutkin G. G. (2008). Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 1783 673–694. 10.1016/j.bbamcr.2008.01.024 PubMed DOI

Yen A. H., Sharpe P. T. (2008). Stem cells and tooth tissue engineering. Cell Tissue Res. 331 359–372. 10.1007/s00441-007-0467-6 PubMed DOI

Yu T., Volponi A. A., Babb R., An Z., Sharpe P. T. (2015). Stem cells in tooth development, growth, repair, and regeneration. Curr. Top. Dev. Biol. 115 187–212. 10.1016/bs.ctdb.2015.07.010 PubMed DOI

Yuan Y., Chai Y. (2019). Chapter Four - Regulatory mechanisms of jaw bone and tooth development. Curr. Top. Dev. Biol. 133 91–118. 10.1016/bs.ctdb.2018.12.013 PubMed DOI PMC

Zhang J., Kawashima N., Suda H., Nakano Y., Takano Y., Azuma M. (2006). The existence of CD11c+ sentinel and F4/80+ interstitial dendritic cells in dental pulp and their dynamics and functional properties. Int. Immunol. 18 1375–1384. 10.1093/intimm/dxl070 PubMed DOI

Zhao Y., Bower A. J., Graf B. W., Boppart M. D., Boppart S. A. (2013). Imaging and tracking of bone marrow-derived immune and stem cells. Methods Mol. Biol. 1052 57–76. 10.1007/7651_2013_28 PubMed DOI PMC

Zhou T., Pan J., Wu P., Huang R., Du W., Zhou Y., et al. (2019). Dental follicle cells: roles in development and beyond. Stem Cells Int. 2019:9159605. 10.1155/2019/9159605 PubMed DOI PMC

Zvackova I., Matalova E., Lesot H. (2017). Regulators of collagen fibrillogenesis during molar development in the mouse. Front. Physiol. 8:554. 10.3389/fphys.2017.00554 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...