Comparative transcriptome profiles of human dental pulp stem cells from maxillary and mandibular teeth.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
25 05 2022
25 05 2022
Historique:
received:
30
01
2022
accepted:
11
05
2022
entrez:
25
5
2022
pubmed:
26
5
2022
medline:
28
5
2022
Statut:
epublish
Résumé
The molecular control of tooth development is different between the maxilla and mandible, contributing to different tooth shapes and locations; however, whether this difference occurs in human permanent teeth is unknown. The aim of this study was to investigate and compare the transcriptome profiles of permanent maxillary and mandibular posterior teeth. Ten participants who had a pair of opposing premolars or molars extracted were recruited. The RNA obtained from cultured dental pulp stem cells underwent RNA-sequencing and qRT-PCR. The transcriptome profiles of two opposing premolar pairs and two molar pairs demonstrated that the upper premolars, lower premolars, upper molars, and lower molars expressed the same top-ranked genes, comprising FN1, COL1A1, COL1A2, ACTB, and EEFIA1, which are involved in extracellular matrix organization, immune system, signal transduction, hemostasis, and vesicle-mediated transport. Comparative transcriptome analyses of each/combined tooth pairs demonstrated that PITX1 was the only gene with different expression levels between upper and lower posterior teeth. PITX1 exhibited a 64-fold and 116-fold higher expression level in lower teeth compared with their upper premolars and molars, respectively. These differences were confirmed by qRT-PCR. Taken together, this study, for the first time, reveals that PITX1 is expressed significantly higher in mandibular posterior teeth compared with maxillary posterior teeth. The difference is more evident in the molars compared with premolars and consistent with its expression pattern in mouse developing teeth. We demonstrate that differences in lower versus upper teeth gene expression during odontogenesis occur in permanent teeth and suggest that these differences should be considered in molecular studies of dental pulp stem cells. Our findings pave the way to develop a more precise treatment in regenerative dentistry such as gene-based therapies for dentin/pulp regeneration and regeneration of different tooth types.
Identifiants
pubmed: 35614192
doi: 10.1038/s41598-022-12867-1
pii: 10.1038/s41598-022-12867-1
pmc: PMC9133121
doi:
Substances chimiques
RNA
63231-63-0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8860Informations de copyright
© 2022. The Author(s).
Références
Martin, K. J. et al. Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles. Proc. Natl. Acad. Sci. 113, 14769–14774 (2016).
pubmed: 27930309
pmcid: 5187730
doi: 10.1073/pnas.1612354113
Rasch, L. J. et al. An ancient dental gene set governs development and continuous regeneration of teeth in sharks. Dev. Biol. 415, 347–370 (2016).
pubmed: 26845577
doi: 10.1016/j.ydbio.2016.01.038
Schmalz, G., Widbiller, M. & Galler, K. M. Clinical perspectives of pulp regeneration. J. Endod. 46, S161–S174 (2020).
pubmed: 32950188
doi: 10.1016/j.joen.2020.06.037
Volponi, A. A., Zaugg, L. K., Neves, V., Liu, Y. & Sharpe, P. T. Tooth repair and regeneration. Curr. Oral Health Rep. 5, 295–303 (2018).
doi: 10.1007/s40496-018-0196-9
Chen, Q. et al. Special at-rich sequence-binding protein 2 (satb2) synergizes with bmp9 and is essential for osteo/odontogenic differentiation of mouse incisor mesenchymal stem cells. Cell Prolif. 54, e13016 (2021).
pubmed: 33660290
pmcid: 8016638
doi: 10.1111/cpr.13016
Zaugg, L. et al. Translation approach for dentine regeneration using gsk-3 antagonists. J. Dent. Res. 99, 544–551 (2020).
pubmed: 32156176
doi: 10.1177/0022034520908593
Da Rosa, W., Piva, E. & Da Silva, A. Disclosing the physiology of pulp tissue for vital pulp therapy. Int. Endod. J. 51, 829–846 (2018).
pubmed: 29405371
doi: 10.1111/iej.12906
Square, T. A., Sundaram, S., Mackey, E. J. & Miller, C. T. Distinct tooth regeneration systems deploy a conserved battery of genes. EvoDevo 12, 4 (2021).
pubmed: 33766133
pmcid: 7995769
doi: 10.1186/s13227-021-00172-3
Jung, C., Kim, S., Sun, T., Cho, Y.-B. & Song, M. Pulp-dentin regeneration: Current approaches and challenges. J. Tissue Eng. 10, 2041731418819263 (2019).
pubmed: 30728935
pmcid: 6351713
doi: 10.1177/2041731418819263
Pantalacci, S. et al. Transcriptomic signatures shaped by cell proportions shed light on comparative developmental biology. Genome Biol. 18, 29 (2017).
pubmed: 28202034
pmcid: 5312534
doi: 10.1186/s13059-017-1157-7
Depew, M. J., Lufkin, T. & Rubenstein, J. L. Specification of jaw subdivisions by dlx genes. Science 298, 381–385 (2002).
pubmed: 12193642
doi: 10.1126/science.1075703
Krivanek, J. et al. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat. Commun. 11, 4816 (2020).
pubmed: 32968047
pmcid: 7511944
doi: 10.1038/s41467-020-18512-7
Olley, R. et al. Expression analysis of candidate genes regulating successional tooth formation in the human embryo. Front. Physiol. 5, 1–8 (2014).
doi: 10.3389/fphys.2014.00445
Azzaldeen, A., Watted, N., Mai, A., Borbély, P. & Abu-Hussein, M. Tooth agenesis; aetiological factors. J. Dent. Med. Sci. 16, 75–85 (2017).
Cunha, A. S. et al. Genetic variants in tooth agenesis-related genes might be also involved in tooth size variations. Clin. Oral Investig. 25, 1307–1318 (2020).
pubmed: 32648061
doi: 10.1007/s00784-020-03437-8
Metzker, M. L. Sequencing technologies—The next generation. Nat. Rev. Genet. 11, 31 (2010).
pubmed: 19997069
doi: 10.1038/nrg2626
Wang, Z., Gerstein, M. & Snyder, M. Rna-seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57–63 (2009).
doi: 10.1038/nrg2484
pubmed: 19015660
pmcid: 2949280
Li, J. et al. Comparison of microarray and RNA-Seq analysis of mRNA expression in dermal mesenchymal stem cells. Biotechnol. Lett. 38, 33–41 (2016).
pubmed: 26463369
doi: 10.1007/s10529-015-1963-5
Hong, M. et al. RNA sequencing: New technologies and applications in cancer research. J. Hematol. Oncol. 13, 166 (2020).
pubmed: 33276803
pmcid: 7716291
doi: 10.1186/s13045-020-01005-x
Tran, T. Q. & Kioussi, C. Pitx genes in development and disease. Cell. Mol. Life Sci. 78, 4921–4938 (2021).
pubmed: 33844046
doi: 10.1007/s00018-021-03833-7
Laugel-Haushalter, V. et al. Molars and incisors: Show your microarray ids. BMC Res. Notes 6, 113 (2013).
pubmed: 23531410
pmcid: 3658942
doi: 10.1186/1756-0500-6-113
Mitsiadis, T. A. & Drouin, J. Deletion of the pitx1 genomic locus affects mandibular tooth morphogenesis and expression of the barx1 and tbx1 genes. Dev. Biol. 313, 887–896 (2008).
pubmed: 18082678
doi: 10.1016/j.ydbio.2007.10.055
Ramanathan, A., Srijaya, T. C., Sukumaran, P., Zain, R. B. & Kasim, N. H. A. Homeobox genes and tooth development: Understanding the biological pathways and applications in regenerative dental science. Arch. Oral Biol. 85, 23–39 (2018).
pubmed: 29031235
doi: 10.1016/j.archoralbio.2017.09.033
Kadler, K. E., Hill, A. & Canty-Laird, E. G. Collagen fibrillogenesis: Fibronectin, integrins, and minor collagens as organizers and nucleators. Curr. Opin. Cell Biol. 20, 495–501 (2008).
pubmed: 18640274
pmcid: 2577133
doi: 10.1016/j.ceb.2008.06.008
Hu, S., Parker, J. & Wright, J. T. Towards unraveling the human tooth transcriptome: The dentome. PLoS One 10, e0124801 (2015).
pubmed: 25849153
pmcid: 4388651
doi: 10.1371/journal.pone.0124801
Liu, X. et al. Regulation of fn1 degradation by the p62/sqstm1-dependent autophagy–lysosome pathway in hnscc. Int. J. Oral Sci. 12, 1–11 (2020).
doi: 10.1038/s41368-020-00101-5
Linde, A., Johansson, S., Jonsson, R. & Jontell, M. Localization of fibronectin during dentinogenesis in rat incisor. Arch. Oral Biol. 27, 1069–1073 (1982).
pubmed: 6763861
doi: 10.1016/0003-9969(82)90013-9
Saito, K. et al. Interaction between fibronectin and β1 integrin is essential for tooth development. PLoS One 10, e0121667 (2015).
pubmed: 25830530
pmcid: 4382024
doi: 10.1371/journal.pone.0121667
Pellenc, D., Berry, H. & Gallet, O. Adsorption-induced fibronectin aggregation and fibrillogenesis. J. Colloid Interface Sci. 298, 132–144 (2006).
pubmed: 16375913
doi: 10.1016/j.jcis.2005.11.059
Winning, L., El Karim, I. A. & Lundy, F. T. A comparative analysis of the osteogenic potential of dental mesenchymal stem cells. Stem Cells Dev. 28, 1050–1058 (2019).
pubmed: 31169063
doi: 10.1089/scd.2019.0023
Xiong, Y. et al. Wnt production in dental epithelium is crucial for tooth differentiation. J. Dent. Res. 98, 580–588 (2019).
pubmed: 30894046
doi: 10.1177/0022034519835194
Schröder, A. et al. Expression kinetics of human periodontal ligament fibroblasts in the early phases of orthodontic tooth movement. J. Orofac. Orthop. 79, 337–351 (2018).
pubmed: 30019109
doi: 10.1007/s00056-018-0145-1
Andersson, K. et al. Mutations in COL1A1 and COL1A2 and dental aberrations in children and adolescents with osteogenesis imperfecta—A retrospective cohort study. PLoS One 12, e0176466 (2017).
pubmed: 28498836
pmcid: 5428910
doi: 10.1371/journal.pone.0176466
Nutchoey, O. et al. Phenotypic features of dentinogenesis imperfecta associated with osteogenesis imperfecta and COL1A2 mutations. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 131, 694–701 (2021).
pubmed: 33737018
doi: 10.1016/j.oooo.2021.01.003
Intarak, N. et al. Tooth ultrastructure of a novel COL1A2 mutation expanding its genotypic and phenotypic spectra. Oral Dis. 27, 1257–1267 (2021).
pubmed: 32989910
doi: 10.1111/odi.13657
Budsamongkol, T. et al. A novel mutation in COL1A2 leads to osteogenesis imperfecta/Ehlers–Danlos overlap syndrome with brachydactyly. Genes Dis. 6, 138–146 (2019).
pubmed: 31193991
pmcid: 6545454
doi: 10.1016/j.gendis.2019.03.001
Eimar, H. et al. Craniofacial and dental defects in the Col1a1
pubmed: 26951553
doi: 10.1177/0022034516637045
Vedula, P. et al. Diverse functions of homologous actin isoforms are defined by their nucleotide, rather than their amino acid sequence. Elife 6, e31661 (2017).
pubmed: 29244021
pmcid: 5794254
doi: 10.7554/eLife.31661
Bunnell, T. M., Burbach, B. J., Shimizu, Y. & Ervasti, J. M. Β-actin specifically controls cell growth, migration, and the g-actin pool. Mol. Biol. Cell 22, 4047–4058 (2011).
pubmed: 21900491
pmcid: 3204067
doi: 10.1091/mbc.e11-06-0582
Abbas, W., Kumar, A. & Herbein, G. The eef1a proteins: At the crossroads of oncogenesis, apoptosis, and viral infections. Front. Oncol. 5, 1–10 (2015).
doi: 10.3389/fonc.2015.00075
Duman, M. et al. Eef1a1 deacetylation enables transcriptional activation of remyelination. Nat. Commun. 11, 3420 (2020).
pubmed: 32647127
pmcid: 7347577
doi: 10.1038/s41467-020-17243-z
Manaspon, C. et al. Human dental pulp stem cell responses to different dental pulp capping materials. BMC Oral Health 21, 1–13 (2021).
doi: 10.1186/s12903-021-01544-w
Porntaveetus, T. et al. Dental properties, ultrastructure, and pulp cells associated with a novel dspp mutation. Oral Dis. 24, 619–627 (2018).
pubmed: 29117466
doi: 10.1111/odi.12801
Sriwattanapong, K. et al. Reduced ELANE and SLPI expression compromises dental pulp cell activity. Cell Prolif. 54, e13132 (2021).
pubmed: 34580954
pmcid: 8560611
doi: 10.1111/cpr.13132
Nowwarote, N. et al. Pten regulates proliferation and osteogenesis of dental pulp cells and adipogenesis of human adipose-derived stem cells. Oral Dis. https://doi.org/10.1111/odi.14030 (2021).
doi: 10.1111/odi.14030
pubmed: 34558757
Gillespie, M. et al. The reactome pathway knowledgebase 2022. Nucleic Acids Res. 50, D687–D692 (2021).
pmcid: 8689983
doi: 10.1093/nar/gkab1028